Volume 71, Number 1 - Suppl., 2011

Editorial Board Takako Matsumura-Tundisi (Editor-in-chief) André Moldenhauer Peret Angelo Antonio Agostinho Catarina Satie Takahashi Denise de Campos Bicudo Donato Seiji Abe Ernesto J. Gonzáles Rivas Flávio Henrique Silva Fernando Rosado Spilki Guillermo Chalar Marquisá Ima Célia Guimarães Vieira José Antonio Mendes José Galizia Tundisi Katherine Vammen Liliana Forneris Marcelo Augusto Marretto Esquisatto Marcos Gomes Nogueira Odete Rocha

Editorial Assistant Rogério Flávio Pessa

Proofreading Chloe Furnival Copyright Published by International Institute of Ecology, a business unit of The International Institute of Ecology, Inc., 750 Rua Bento Carlos, São Carlos, SP - . Copyright © 2005 by The International Institute of Ecology, Inc. All rights reserved. No part of this publication may be reproduced or distributed in any form or by any means, or stored in a database or retrieval system, without the prior written consent of The International Institute of Ecology, Inc., including but not limited to, in any network or other eletronic storage or transmission, or broadcast for distance learning. Some ancillaries, including eletronic and print components, may not be available to customers outside.

Revista Brasileira de Biologia / Brazilian Journal of Biology® Vol. 1, n. 1 (abr. 1941) Quaterly published Text and abstract in english; abstract in portuguese Printed with support of ASRBB® and Universidade Anhanguera/Uniderp.

ISSN 1519-6984 1. Ecology 2. Zoology 3. Botany 4. Celular Biology

Online version: www.scielo.br/bjb

Cover illustration:

• Local: Ninhal and corixo - Pantanal - Brazil • Photografed by: Ricardo Zig Koch Cavalcanti/Banco de Imagens ANA (Agência Nacional de Águas)

Graphics production: Desktop publishing and cover art:

April, 2011 Volume 71, Number 1 - Suppl., 2011

Guest Editors Cleber J. R. Alho (Editor-in-chief) Elizabeth Teresa Brunini Sbardelini Eva Teixeira dos Santos Silvio Favero Ademir Kleber Morbeck de Oliveira Mercedes Abid Mercante José Sabino

ISSN 1519-6984

Brazilian Journal of Biology®

VOLUME 71 APRIL, 2011 NUMBER 1 - SUPPL.

EDITORIAL NOTE

Among the wetlands of Brazil, the Pantanal occupies a very important position. With its almost 200,000 km2, this tropical wetland harbours a diverse flora and fauna which is a result of the intensive interactions of flooding in rivers, lakes, natural channels, creeks and streams. Knowledge ofthe Pantanal biodiversity is of prime importance for its conservation and the identification of the ecosystem services of this large wetland. This volume constitutes an effort to characterise the Pantanal´s biodiversity and it is one more contribution from the Brazilian Journal of Biology to improve knowledge on Neotropical biodiversity.

The Editorial Board

PRESENTATION

The United Nations has declared 2010 the “International Year of Biodiversity”, to celebrate biological diversity and emphasise its importance in our lives. Brazil is one of the signatories of the Convention on Biological Diversity and is implementing its recommendations towards conservation and sustainable use of its territory. Additionally, the United Nations General Assembly declared 2011 as the International Year of Forests to raise awareness on sustainable management, conservation and sustainable development of all types of forests. The Pro-reitoria de Pesquisa e Pós-graduação (responsible for graduate studies and research) of the Anhanguera/Uniderp university is proud to give its shared support, along with the Instituto Internacional de Ecologia (International Institute of Ecology -IIE), in producing this special number of the Revista Brasileira de Biologia (Brazilian Journal of Biology) on the Biodiversity of the Pantanal. It aims to provide unified scientific information, secure regional academic contributions and improve the conservation of our important neighbouring biome. Authors include researchers from different institutions of our region as well as from national agencies. The volume is organised to emphasise scientific and cultural knowledge on biodiversity, focussing on its conservation under natural circumstances. The focus on biodiversity reflects the increasing interest and concern among Brazilian academics and the general public for the importance of the diversity of life within the Pantanal. This increased motivation and attention are expressed in the Brazilian Constitution of 1988, declaring the biome a National Heritage Area, as well as the international recognition with the declaration of Wetland of International Importance under the Convention on Wetlands (RAMSAR), and as a Biosphere Reserve, granted by the United Nations Educational, Scientific and Cultural Organization (UNESCO). This volume brings together a number of articles expressing different views on a diverse array of subjects as a collaborative action for the same purpose: emphasising the value of academic research for increased knowledge about the richness of and natural conservation. The main message of this special volume is to stress the benefits of knowing and conserving the Pantanal’s biota, which our society cannot afford to lose. Scientists, the media, and the public in general are aware of the many convincing arguments for the importance of our biodiversity. Individual attitudes are important, but institutional action, which motivates the publication of this volume, contributes to our placing a higher value on biology, from molecules to ecosystems, and to avoiding the tragedies associated with species loss. The 200th anniversary of Charles Darwin’s birth, celebrated on 12 February of 2009, was a gratifying event, given his position as the father of modern biology; his theory of evolution and the broader principle of natural selection are strikingly present in the Pantanal’s biodiversity. His celebrated Origin of Species serves as a stimulus, reminding us how powerfully a publication brings insights and practical benefits together towards a more hopeful future for protected nature.

Prof. Dr. Guilherme Marback Neto President (Rector) University Anhanguera/Uniderp, Campo Grande, , Brazil

OVERVIEW: EDITOR’S FOREWORD

Biodiversity of the Pantanal: its magnitude, human occupation, environmental threats and challenges for conservation Alho, CJR.* Programa de Pós-graduação em Meio Ambiente e Desenvolvimento Regional, Universidade Anhanguera – Uniderp, Rua Alexandre Herculano, 1400, CEP 79037-280, Campo Grande, MS, Brazil *e-mail: [email protected] Received October 14, 2010 – Accepted December 13, 2010 – Distributed April 30, 2011

The Pantanal biome is a wetland – a floodplain in a Fish. Fish are an important resource, both ecologically geographic depression – formed by the River and and socially. Britiski et al. (1999) listed 263 species for its tributaries from the left bank: Bento Gomes, Cuiabá, the Pantanal. However, a survey carried out in the Negro São Lourenço-Itiquira, Taquari, Negro, Aquidauana- River region of the Pantanal showed that 19% of the species Miranda, Nabileque, and Apa. The Paraguay River and collected are believed to be new to science (Willink et al., its tributaries form the Upper Paraguay Basin and drain 2000). This list does not include species living in the upper into the Pantanal depression, running southward between river . The number of fish species increases from highlands to the west and the upland plateaus to the east, the headwaters (plateau upland region or planalto) to the where the tributaries have their springs. These large rivers base of the drainage (Pantanal). are shaped largely by type of soil, water flow rate, levels Because of the great variety of feeding and reproductive of dissolved oxygen, nutrient loads, temperature, and type niches for fish, the Pantanal harbours high species abundance. of river bed. The rivers are slow moving when they leave Fishing is of fundamental social-economic importance for the upland plateaus surrounding the floodplain and meet local people. In addition, fishing for sport is one of the the flatlands, where they periodically overflow their banks. incentives to bring tourists to the region. Junk et al. (2006) The maze of fluctuating water levels within this discuss more on fish diversity of the Pantanal. sedimentary floodplain, plus annual nutrient cycling Fish resources in the Pantanal have been recognised though biogeochemical cycles with influx of nutrients, according to their use as: particulate material, microorganisms and invertebrates • a fundamental biotic component of the ecosystem, form a dynamic ecosystem, with a complex mosaic of supporting the local biodiversity and being habitats and diverse and abundant wildlife. The four part of it; phases of the hydrological cycle (water rising or flooding, • food for subsistence and income of local people; flood season, receding water or drainage season, and dry • of interest for sport fishing; season) are essential for wildlife. The annual tides of the • a genetic resource; rivers, causing seasonal flooding, result in availability of • an ornamental resource. feeding and reproductive niches for wildlife. Herpetofauna. Compared to other Brazilian biomes, Macroinvertebrates. The diversity of benthonic the Pantanal presents a herpetofauna low in diversity but macroinvertebrates (zoobenthos such as decapods, molluscs, high in abundance. There are 135 herpetofaunal species oligochaetes, insect larvae which feed upon microoganisms living on the plains (40 species of anuran , and algae) were estimated in 70 taxa (Takeda et al., 2000). three species of turtles, 25 species of lizards, two species Zoobenthos are important in the food chain because they of amphisbaenians, 63 species of and two of serve as food for fish, birds, mammals and other crocodilians (Junk et al., 2006). A survey carried out in groups. Ostracoda (aquatic crustacea) and Nematoda the southern Pantanal recorded 41 anuran and 24 (free living non-parasitic roundworms) are the two most species (Strüssman et al., 2000). abundant groups. During the rainy season the region presents vigorous Crustacean diversity. Shrimps and crabs are represented populations of amphibians, thanks to the expansion of by 10 species and the shrimp Macrobrachium amazonicum favourable habitats. Three reproductive activity patterns and the crabs Dilocarcinus pagei, Sylviocarcinus australis, are recognised among the species: continuous, explosive, Trichodactylus borellianus and Valdivia camerani are and prolonged; 50% of the species were explosive breeders found in field surveys (Magalhães, 2000). These decapod (Prado, 2003). crustaceans play an important role in ecological processes Many Pantanal species are distributed throughout of the Pantanal’s aquatic ecosystem since they participate Brazil, such as the rococo-toad Bufo paracnemis and the in the trophic chain as herbivores, predators, decomposers Chaco- Leptodactylus chaquensis, the dwarf-tree and are prey for fish and other animal groups. Hyla fuscovaria; Hyla acuminata, Hyla raniceps, the diversity. Three articles discussing of the green-leaf-frog acuminatus, the marbled-tree-frog Pantanal are presented in this volume. Phrynohyas venulosa and the common-washroom-frog

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 229-232 229 Alho, CJR.

Scinax cf. nasicus. The abundant tine green frog Lysapus observed for amphibians, but with difference in local limellus has a semi-aquatic habit, lives on floating plants, abundance, which is more remarkable in the Pantanal for eating insects and other invertebrates (Alho et al., 2002). these species. About half of the anuran species in the Pantanal There is one terrestrial turtle, the red-footed-tortoise live in trees. Some species, such as the spotted-tree-frog Geochelone carbonaria plus one aquatic species, the Hyla punctata, are associated with permanent bodies large-headed-Pantanal-swamp-turtle Acanthochelys of water (rivers and ponds) and others, such as the macrocephala. The caiman Caiman crocodillus is abundant purple‑barred-tree‑frog Hyla raniceps, the green-leaf‑frog and conspicuous, particularly during the dry season, being Scinax acuminatus, the yellow-and-black-tree-frog Scinax one of the symbols of the Pantanal. fuscovarius, tolerate droughts but the population suddenly Twenty species of lizards are known for the region, all grows when flooding comes, usually October to May. preferring dry habitats except for the Pantanal-caiman-lizard Frogs are also more vocal during this period. Dracaena paraguayensis which lives in the water. Two lizard The tiny clicking-frog Lysapsus limellus lives on floating species, Kentropyx viridistriga and Mabuya guaporicola, vegetation and also vocalises by day. Also vocalising on are able to swim and dive to escape predators. Common floating plants are the paradox-frog paradoxa geckos, Phyllopezus policaris and Polychrus acutirostris, and the speckled-bellied-frog albonotatus. exploit the branches of bushes. Three lizards can be easily During the rainy season this Physalaemus albonotatus observed searching for prey on the ground or rapidly frog is one of the most conspicuous and vocal when they escaping from intruders: Tupinambis merianae, Ameiva join in sonorous choir, even by day. ameiva and Cnemidophorus ocellifer. The green‑iguana Amphibians with terrestrial habits are the leaf‑toad Iguana iguana is also seen in trees along the rivers or on Bufo typhonius, the frogs Chiasmocleis mehelyi, Leptodactylus riverbanks. elenae, Physalaemus cuvieri, and the arboreal frog Phrynohyas Bird Diversity. There are 444 bird species recorded venulosa. Another tiny frog living in dead tree holes in the only for the floodplains, 665 species when the uplands are forest is Chiasmocleis mehelyi, which has only recently included and 837 species for the Cerrado biome (Tubelis been reported in the Pantanal. Some other species live at and Tomas, 2002; Silva, 1995). the water line between aquatic and terrestrial habitats, such A bird field guide published in Portuguese “Aves do as Pseudopaludicola aff. falcipes, Leptodactylus fuscus, Brasil: Pantanal & Cerrado” and in English, “Birds of Leptodactylus podicipinus, Bufo paracnemis, Bufo granulosus Brazil: Pantanal & Cerrado” (Gwynne et al., 2010) pointed and Elachistocleis cf. ovale. A colourful aposematic species out 740 species for both biomes highlighting the birdlife is Phyllomedusa hypochondrialis. to inspire bird watching to enjoy the biomes’ vibrant Among , there are more than 30 species of ecosystems and natural heritage, addressing an ecological . The yellow-anaconda Eunectes notaeus is very context an conservation messages. common on the plains and is small in size compared to the More discussion on bird diversity is provided by Junk other species, the green anaconda E. murinus that lives at et al (2006). Bird species with aquatic habits are very the edge of the Pantanal and may reach 5 m in size, some common and abundant, including egrets such as species observations reporting a size of 6-8 m. Another large snake of the genera Casmerodius, Egretta, Ardea, Tigrisoma, is the water-queen Hydrodynastes gigas, which occurs Botaurus, in addition to the wood‑stork Mycteria americana, at the borders of gallery forests or patches of savannas the maguari-stork Ciconia maguari and the jabiru Jabiru looking for toads, their preferred food. Small nocturnal mycteria. Kingfishers are present with 5 species of the two snakes, which prey upon frogs, are Thamnodynastes cf. genera Ceryle and Choroceryle. Other aquatic species are the strigilis, Leptodeira annulata and Liophis poecilogyrus. southern‑screamer Chauna torquata, the muscovy‑duck There are four species of poisonous snakes in the Cairina moschata, the fulvous‑whistling‑duck Dendrocygna Pantanal: the Brazilian-lancehead Bothrops moojeni, the bicolor, the white‑faced‑whistling-duck D. viduata, the Neuwid’lancehead B. neuwiedi, the neotropical-rattlesnake black‑bellied‑whistling‑duck D. autumnalis and the Crotalus durissus and the Pantanal-coral-snake Micrurus Brazilian‑duck Amazonetta brasilienses. Among birds tricolor. of prey are the snail-kite Rosthramus sociabilis, the The occurrence of species within the sub-regions of the black‑collared‑hawk Busarellus nigricollis, the Pantanal varies according to the local species composition great‑black‑hawk Butteogallus urubitinga and the Crane‑hawk and distribution, depending on the influence of the nearby Geranospiza caerulescens. Parrots are abundant. I observed biomes such as the Chaco, the Cerrado and the Amazonia. a group of 206 turquoise‑fronted-parrots Amazona aestiva Among the snakes of the northern sub-region of Poconé, in the SESC Reserve at Barão de Melgaço. There are for example, Strüssmann and Sazima (1993) observed 19 species of psitasids including the hyacinth macaw that the most abundant species are Eunectes notaeus, Anodorhynchus hyacinthinus. Helicops leopardinu and Hydrodynastes cf strigilis. While Conservation. The biome’s biodiversity has been the southern sub-region of Nhecolândia presented different impacted by unsustainable socio-economic practices, species composition with Leptodeira annulata, Liophis including: typhlus and Lystrophis mattogrossensis, snakes common • deforestation (conversion of natural vegetation throughout the Brazilian Cerrado. The same pattern is into pastures for cattle, conversion of Cerrado

230 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 229-232 Pantanal’s biodiversity: magnitude and threats

vegetation into crop fields in the uplands where the Pantanal. The working structure of INAU the headwaters are located, charcoal production, facilitates the integration of the Pantanal Research habitat loss and alteration); data on deforestation Center (CPP) and the Universidade Federal de of the Pantanal biome for the period 1976-2008 Mato Grosso (Federal University of Mato Grosso) show about 15% of natural vegetation loss with in Cuiabá; degradation reaching near 60% in the surrounding • NGO’s ACTION PLANS – Different NGOs uplands (Silva et al., 2010); play important role on biodiversity conservation • environmental contaminants (petroleum-based of the Pantanal. For example, the diagnosis inputs of agricultural chemicals, mainly in the entitled “Monitoring Alterations in Vegetation and uplands, mercury contamination in gold mining, Land Use in the Brazilian Portion of the Upper in addition to iron ore, manganese, and calcium Paraguay River Basin” was carried out by the carbonate, sewage and domestic waste from nongovernmental organizations: Ecoa - Ecologia the great majority of the cities surrounding the e Ação, Conservation International, Avina Pantanal); Foundation, SOS Pantanal and WWF ‑ Brasil • infrastructure and unplanned human occupation and received technical support from Embrapa (large cargo convoys navigate the large rivers of Pantanal. The purpose of the study was to make the Pantanal, mainly the Paraguay and Cuiabá a detailed analysis of changes in vegetation rivers, and vessels damage riverbanks with oil patterns and land use that took place in the spills and waste; road kills of wildlife along roads period from 2002 to 2008. The diagnostic study throughout the wetlands); shows that compared to other Brazilian biomes • unregulated tourism (predatory invasion of like the Atlantic Forest formations, the Pantanal waterfowl nesting grounds, sport fishing with is relatively well-conserved although it is very illegal campsites in gallery forests spreading vulnerable especially to impacts occurring in the waste); highland regions of the Upper Paraguay River • fragility of law enforcement (some protected basin. While the lower floodplain region has areas, hunting activities, commercial and sport 86.6% of its natural vegetation cover intact, only fishing, deforestation with soil degradation are 43.5% of the highland plateau areas have their generally out of the control of the environmental original vegetation; agencies, with consequent impacts on habitats and • ACADEMIC CONTRIBUTIONS – Regional biodiversity loss); Universities such as the UFMT (Universidade • introduction of exotic species (there are a Federal do Mato Grosso = Federal University of considerable number of introduced species within Mato Grosso); the UFMS (Universidade Federal the natural habitats, both deliberate and accidental: do Mato Grosso do Sul = Federal University tucunaré fish, feral pig, Limnoperma fortunei of Mato Grosso do Sul), the state Universities mussel and others). for both states, and private universities like The major economic activities in terms of land occupation the Anhanguera-Uniderp (Universidade para are cattle ranching and tourism. Many large ranches have o Desenvolvimento do Estado e da Região do been subdivided into small farms, modifying the original Pantanal = University for the Development of arrangement of extensive cattle ranching. In recent years, the State and the Region of the Pantanal) are over-fishing has been seen to be a major problem in the contributing with academic research including region. thesis and dissertations; Some major projects and studies have been carried out: • CPAP (Embrapa Pantanal = Embrapa Pantanal • The EDIBAP (Study for the Integrated Research Center) of Embrapa (Empresa Brasileira Development of the Upper Paraguay River Basin), de Pesquisa Agropecuária = Brazilian Agricultural between 1977 and 1989; Research Corporation) – The Center was implanted • The PCBAP (Plan for Conservation of the Upper in Corumbá in 1975. Its mission is to make Paraguay Basin), conducted in 1997; technological solutions viable for the sustainable • The ANA/GEF/UNEP/OAS (Strategic Action development of the Pantanal agribusiness with the Program for the Integrated Management of the valorization of nature, including fauna and flora Pantanal and the Upper Paraguay River Basin), conservation; carried out by ANA (Brazilian National Water • There have been different programmes and Agency) in 2005; activities to establish initiatives to identify critical • INAU – Instituto Nacional de Ciência e priorities for the conservation of biodiversity, Tecnologia em Áreas Úmidas (The National including the creation of new protected areas. Institute of Science and Technology in Wetlands). The conservation strategy should consider the This new institute aims to carry out research to Pantanal as a whole biome, connecting all sub- support public policies for the conservation and regions and different ecosystems, with protected sustainable management of natural resources in areas representative of the major sub-region, as

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well as considering the role of ecological corridors Paulista, Campus de Rio Claro. 150 p. Tese de doutorado em for the dispersion of species and integration of the zoologia. adjacent biomes. SILVA, JSV., ABDON, MM., MORAES, JA., 2010. Desmatamento The challenge for conservation of the magnificent na bacia do Alto Paraguai no Brasil. In Anais 3º Simpósio de biodiversity of the Pantanal increases as time passes and, Geotecnologias no Pantanal. Cáceres, MT, 16-20 de outubro unfortunately, we can testify to the loss of habitats and 2010. Embrapa Informática Agropecuária/INPE, p. 459-467. species, not as a result of natural selection, but because of SILVA, JMC., 1995. Birds of the cerrado region, . human disturbance. If on the one hand scientific knowledge Steenstrupia, no. 21, p. 69-92. is fundamental for the implementation of conservation, on the other hand, scientific results alone cannot solve the STRÜSSMAN, C., PRADO, CPA., UETANABARO, M. and FERREIRA, VL., 2000. and reptile survey of selected problems of environmental disruption. However, we are localities in the southern Pantanal floodplains and surrounding convinced that the scientific information available in this cerrado, Mato Grosso do Sul, Brasil. In: Philip W. Willink, special number of the Brazilian Journal of Biology will Barry Chernoff, Leeanne E. Alonso, Jensen R. Montambault and play a vital role in conserving the regional biodiversity Reinaldo Lourival (eds.). A biological assessment of the aquatic of the Pantanal biome. It will add important scientific ecosystems of the Pantanal, Mato Grosso do Sul, Brasil. RAP knowledge to environmental awareness, providing a basis Bulletin of Biological Assessment 18. Conservation International, for government action and encouraging us all to practise Washington DC. humanitarian values to protect our natural treasures through STRUSSMANN, C. and SAZIMA, I., 1993. The snake assemblage ethical attitudes. of the Pantanal at Pocone, Western Brazil: faunal composition and ecological summary. Studies on Neotropical Fauna and References Environment, vol. 28, no., 3, p. 157-168. TAKEDA, A., PEREIRA, MCF. and BARBOSA, FAR., 2000. ALHO, CJR., STRÜSSMANN, C. and VASCONCELLOS, LS., Zoobenthos survey of the Pantanal, Mato Grosso do Sul, Brasil. 2002. Indicadores da magnitude da diversidade e abundância In PHILIP, WW., BARRY, C., LEEANNE, EA., JENSEN, RM. de vertebrados silvestres do Pantanal num mosaico de hábitats AND REINALDO, L., Ed., 2000. A biological assessment of the sazonais. Corumbá, MS: Centro de Pesquisa Agro-Pecuária da aquatic ecosystems of the Pantanal, Mato Grosso do Sul, Brasil. EMBRAPA. Washington, D.C.: Conservation International. RAP Bulletin of Biological Assessment, 18. BRITISKI, MA., SILIMON, KZ. and BALZAC, SL., 1999. Peixes do Pantanal. Manual de identificação. Corumbá: EMBRAPA- TUBELIS, DP. and TOMÁS, WM., 2002. Caracterização da CPAP. 184 p. avifauna da planicie do Pantanal. Indicadores da magnitude da diversidade e abundância de vertebrados silvestres do Pantanal GWYNNE, JA., RIDGELY, RS., TUDOR, G. and ARGEL, M., num mosaico de hábitats sazonais. Corumbá, MS: Centro de 2010. Aves do Brasil – Pantanal & Cerrado. São Paulo: Wildlife Pesquisa Agro-Pecuária da EMBRAPA. Conservation Society, Ed. Horizonte. 322 p. JUNK, WJ., CUNHA, CN., WANTZEN, KM., PETERMANN, WILLINK, P. et al., 2000. Fishes of the rios Negro, Negrinho, P., STRÜSSMANN, C., MARQUES, MI. and ADIS, J., 2006. Taboco, Aquidauana, Taquari, and Miranda, Pantanal, Brasil: Biodiversity and its conservation in the Pantanal of Mato Grosso, diversity, distribution, critical habitats and value. In PHILIP, Brazil. Aquatic Sciences, vol. 68, p. 278-309. WW., BARRY, C., LEEANNE, EA., JENSEN, RM. AND REINALDO, L., Ed., 2000. A biological assessment of the PRADO, CPA., 2003. Estratégias reprodutivas em uma comunidade aquatic ecosystems of the Pantanal, Mato Grosso do Sul, Brasil. de anuros no Pantanal, Estado de Mato Grosso do Sul, Brasil. Washington, D.C.: Conservation International. RAP Bulletin of Rio Claro, SP: Instituto de Biociências da Universidade Estadual Biological Assessment, 18.

232 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 229-232 Geomorphology and habitat diversity in the Pantanal Mercante, MA.a*, Rodrigues, SC.b* and Ross, JLS.c* aPrograma de Pós-graduação em Meio Ambiente e Desenvolvimento Regional, Universidade Anhanguera – Uniderp, Rua Alexandre Herculano, 1400, Jardim Veraneio, CEP 79037-280, Campo Grande, MS, Brazil bInstituto de Geografia, Universidade Federal de Uberlândia – UFU, Av. João Naves de Ávila, 2121, CEP 38400-902, Uberlândia, MG, Brazil cDepartamento de Geografia, Faculdade de Filosofia, Letras e Ciências Humanas – FFLCH, Universidade de São Paulo – USP, Av. Lineu Prestes, 338, CEP 05508-970, São Paulo, SP, Brazil *e-mail: [email protected], [email protected], [email protected] Received October 14, 2010 – Accepted December 13, 2010 – Distributed April 30, 2011 (With 4 figures)

Abstract The present study deals with the inter-relations in the relief which forms the Bacia do Alto Rio Paraguay (BAP) in mid‑west Brazil. The overall aim is to discuss the relationship between relief forms and the biodiversity of the Pantanal. The BAP is a natural environmental system with contrasts in two of the compartments on which it is formed: the plateau, the most elevated compartment, highly transformed by human activities, and the plain which forms the Pantanal, which is more preserved and less transformed in relation to productive activities. The analysis was performed based on publications with a geomorphologic focus, examining the different relief units of the BAP and the dynamics of the revealing processes of landscape change which the Pantanal has undergone since the end of the Pleistocene. Keywords: Pantanal geomorphology, biodiversity, relief.

Geomorfologia e a biodiversidade no Pantanal

Resumo O presente estudo tem como objetivo abordar a inter-relação entre os compartimentos do relevo brasileiro que compõem a Bacia do Alto Paraguai - BAP, para discutir as formas de relevo e a biodiversidade do Pantanal. A abordagem fundamenta-se na compreensão das diferentes formas do terreno, associando ao fato que a BAP é um sistema ambiental natural que tem contrastes nos dois compartimentos que a compõem: o planalto, o compartimento mais elevado, fortemente transformado por atividades humanas; e a planície, que constitui o Pantanal mato-grossense, mais conservada e pouco transformada, quanto ao uso com atividades produtivas. A análise foi realizada a partir de publicações com enfoques geomorfológicos, abordando as diferentes unidades do relevo da BAP e o entendimento da dinâmica dos processos reveladores de que o Pantanal passa desde o fim do Pleistoceno, com processos de mudanças da paisagem. Palavras-chave: geomorfologia do Pantanal, biodiversidade, relevo.

1. Introduction Biodiversity itself is a relatively recent term, and it Since relief is the result of endogenous and exogenous has only recently been studied in relation to other areas forces, including climatic and tectonic factors, it helps to of scientific knowledge, such as geomorphology. There explain the distribution, diversity, extinction and performance have been few studies on the biodiversity of the Pantanal of living beings on the earth’s surface (Silva, 1984). Mato-Grossense which deal with the relief forms at the The definition of geomorphologic units is based on the interface of the abiotic, biotic and anthropic components supposition that the planet is the result of the interaction of its complex environmental system (Franco and Pinheiro, between living beings and the physical-geographical 1982; Silva, 1984; Ross, 1990; Ab’Saber, 1996; Alho and environment. This is illustrated in the works of Tricart Gonçalves, 2005). (1972), in the form of a matrix. While the morphogenetic The spatial arrangement of the relief forms is considered processes modify the surface of the Earth they generate an important variable for understanding the diversity of instability and harm the multiple and fragile balances the landscapes and one of the indicators of the dynamic towards which the systems incline, connected by a chain balance in the protection of biodiversity. of interdependences, such as that shown in Figure 1.

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 233-240 233 Mercante, MA., Rodrigues, SC. and Ross, JLS.

region the natural cover represents 42% of the total territory and on the plain the percentage is 87% (Conservação International, 2009; Abdon et al., 2007). Alho (2008, p. 958) provides an analysis of the key factors that have impacted the Pantanal’s ecosystems: The present landscape arrangement and natural ecosystems are the result of three factors: 1) geological changes occurring since the Quaternary, which probably infl uenced the drainage patterns of the region; 2) the pronounced differences in annual cycles of wet and dry seasons plus exceptional periods of long fl ooding or droughts causing retraction or expansion of the Pantanal, thus, a phenomena related to greater or lesser primary productivity and ecological succession and 3) areas related to human intervention such as pastures, artifi cial ponds or introduced trees near the ranch houses. Assine (2003) and Mercante et al. (2007). indicate the existence of complex processes of change in the landscape of the Pantanal, resulting from the sedimentary dynamic in Figure 1. Flow chart elaborated based on Tricart´s alluvial fans. In these fan regions the landscape changes conception (1972). continuously because of sedimentation and by avulsion processes. These cause changes in the river beds, such as those occurring in the Taquari River. The Pantanal is a highly changeable quaternary In the Tricartian matrix the models are situated at the sedimentary plain. Its understanding is vital to projects for use and occupation, as well as conservation and preservation, interface of abiotic, biotic and anthropic components. Tricart and needs to be based on interdisciplinary knowledge considered that an eco-dynamic unit is characterised by a (Ab’Saber, 1988; Alho and Gonçalves, 2005; Assine et al., certain dynamic of the environment and has repercussions 2008; Mercante and Paiva, 2009; Mercante and Santos, on biosinesis. 2009). This study is placed within this context, in order Studies by Ross (2006) have been based on a combination to identify aspects of relief forms which are important to of information about natural vegetation, lithology, relief the biodiversity of the Pantanal Mato-Grossense. First forms, soils, climate and biogeography. These have we examine the relationship between plateau and plain culminated in the mapping of the territorial macrospaces by classifying the compartments and cartography of in Brazil, which also show the different types of land use the relief units. Next, we describe different relief forms by society. in the Pantanal, with special attention to the formation The Ross classifi cation (2006) was built on this of fl uvial fans. Last, some conceptual lessons will be integrated view. Ross’s analysis of the BAP places the highlighted in order to detail the innumerous landscape plateau in the category of savannah that has been highly features that characterise the region’s relief and shelter transformed by economic activities. In contrast, the plain its rich biodiversity. where the Pantanal Mato-Grossense lies is placed in the slightly transformed group of natural environmental systems, 2. Study Area such as the fl uvial plains of Araguaia and Guaporé and some marine plains. The Pantanal, located between parallels 15º and The Pantanal Mato-Grossense is a natural system 20º S and meridians 55º and 59º W, is a vast low fl at presenting a great diversity in fl ora and fauna. Even though plain. It features a depositional tract of sandy sediments it is occupied by human activities, the Pantanal presents derived from the plateaus of sedimentary basins, forming low transformation intensity in the natural vegetation cover huge alluvial fans and lacustrine and fl uvial environments. caused by productive activities such as farming and mining. Accumulation areas are geomorphologically highlighted on the plain with seasonal fl oods and other areas of However, it has undergone very strong impacts from other fl uvio-lacustrine accumulation. activities. The two main threats are the uncontrolled use of The Pantanal Mato-Grossense has worldwide value soil in the areas surrounding the Pantanal plain, which are and is recognised as the world’s largest continuous inland drier and fl ood free; and the consequences of deforestation wetland. It ranges in altitude from 100 to 150 m, presents on the plateau. The latter is a result of many development fl at relief, and lies within a signifi cant geological unit plans for Central Brazil, none of which considered the known as the Bacia do Alto Paraguay (BAP) (Figure 2). natural connection between the high and low parts of the region (Conservação International, 2009). 3. Procedures The plateau is also intensively used for agriculture and cattle breeding. Human occupation is less invasive in We analyse texts and cartographic examples, integrating the natural vegetation cover of the plains. On the plateau methodological focus based on the idea that relief forms are

234 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 233-240 Geomorphology and habitat diversity in the Pantanal

Figure 2. Illustration of the diagram block showing aerial view from West and the flat texture representing the unit of the Pantanal flats and the Pantanal itself and the remaining wrinkled texture representing the surrounding plateau. The inferior part of the illustration shows the topographic profile elaborated from north to south axis starting with the high parts of the plateau followed by the depressed part of the flat and finishing on the plateaus of the extreme south. Adapted from Alho and Gonçalves (2005).

direct and permanent products of the interactions between shapes are important for all living beings, which need a internal and external energy flows. The methodology used physical support, or biotopic. in this study is based on a literature review of publications The relief of the Bacia do Alto Paraguai is marked presenting mappings of the different geomorphologic by the contrast between the plain which is the Pantanal, compartments of the BAP, where we can find the plain with areas ranging from 50 to 150 m above sea level, and and the marshlands of the Paraguay River, known as the the elevated lands of the plateau (200 to 1,200 m above Pantanal Mato-Grossense. sea level). The concepts of Ross (2006) have been adopted for 4.1. Classification and relief units the generation of the BAP map, highlighting the relief According to the classification of the geomorphologic macroforms of the surrounding plateau and including the units of Brazil elaborated by Ross (2006) the plain and Pantanal Mato-Grossense plain. Ross (2006) provides the the Pantanal of the River Paraguay are surrounded to the basis to understand that the Pantanal Mato-Grossense is east, northeast, south and southeast by macroforms of an active sedimentary basin being filled by a considerable Brazilian relief (Figure 3). layer of sediments that come from the surrounding plateau. In the cartographic synthesis with the different He demonstrates that the plain and the marshland are geomorphologic units of the macroforms of Brazilian natural environmental systems which have undergone relief, the plain and the Pantanal of the Paraguay River, little transformation, taking into account information as mapped and denominated by Ross (2006), are one large on the characteristics of natural vegetation, geology, unit considered a slightly transformed environment despite geomorphology, pedology, climate and biogeography. being occupied by human activities. In order to understand the sedimentary processes the The data and information presented in Table 1 reveal studies by Tricart (1972, 1982) were used. These are based one of the important aspects of the Bacia do Alto Paraguay, on the premise that geomorphologic evolution generates which are the relief macroforms which surround the differentiation in the relief units. On the Pantanal Plain, plain and the Pantanal of the Paraguay River. These in particular, the sedimentary dynamics involves the geomorphologic units are important in order to understand formation of alluvial fans. the existing complexity in the processes of accumulation and the fluvial processes on the plain. 4. Discussion 4.2. The plain and the Pantanal of the Paraguay River Relief, as one of the components of the natural The plain represented in Figure 3 as a large white environment, presents a great diversity of shapes. These area presents low intensity of transformation of the

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Caceres

Orion

Rio Paraguay

Três Bocas

N

W E Taquari River Pto S Francisco S Coxim Aluvial fan taquari

Corumba Pto Manga

Nhecolândia

Rio Negro Pto Esperança Rio Aquidauana

Rio Paraguay

Quaternary aluvial Pre-Quaternary Paleochannels fans axes Permanent Lakes Vazantes Paleodunes and Escarpment Temporary marsh paleodepressions - today with colluvium with lakes Permanent marsh 0 50 100 km

Figure 3. It is shown in the cartographic product about the geomorphology of Pantanal, elaborated by Tricart, the design of the alluvial fans, and the observations about the geomorphologic partitioning.

natural vegetation cover by interventions of productive Based on the interpretation of orbital images available activities, such as extensive cattle breeding, subsistence in the 1980s, Tricart (1982) mapped the main areas of past agriculture, fishing, mining and timber extraction. In these action of eolic processes and used cartography to present less transformed environments the natural conditions are the alluvial fans of the Pantanal, whose distributary pattern highly diversified, and mosaic plant cover is formed. There of the rivers were highlighted by the fluvial paleochannels. are various types of words, also highlighted on the map: on The author also analysed geomorphological conditions the wetlands, the fluvial dykes and the uplands known as in the areas with lagoons. He considered that these regions, “cordilheiras”. All these environments are extremely rich nowadays occupied by innumerous circular and semi- in fauna and flora and have been used for many different circular lagoons like those present in the Nhecolândia human activities. Pantanal, are a relic of non-active alluvial fans.

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Table 1. Geomorphologic units in the surrounding of Pantanal Mato-Grossense, based on Ross classification (2006). Adapted from Ross (2006). Paraná basin plateau and lowlands Relief forms Altitude(m) Litology Soils Ample hills with convex 400 - 700 Sandstones Red-yellow-sandy latosoils summits – mid-north. 700 - 800 Sandstones associated Sandy-red claysoils Chapadas – flat surfaces on 500 - 1,400 with clayish detritical Clayish red latosoils the North-Northeast Patamares covering Nitosoil cambic soils, litolic and structural scarps associated Basalts, diabases and to hills and mound-hills with rhyolite. convex summits. Scarps on the edges Alto Paraguai Plateau and residual elevations Elongated elevations on 600 - 800 Calcareous silicified Litolic neosoil anticlinal crystals – synclinal – 300 - 400 sandstone Cambic neosoil mountainous relief 200 - 300 Shales Rocky outcrops Valleys and closed anticlinal arkose Red claysoils depressions Ample synclinal valleys Intermountain depressions Bodoquena Plateau Surfaces of hills with convex 600 - 900 Migmatite, gneisses, Red claysoils summits, fragments with flat amphybolite, quartzite, Litolic neosoil summits carbonatic rocks and granites Cuiabana Depression Vast mound-hills with slightly 150 - 400 Metasandstones – Red-yellow plintosoils and carved valleys phyllite – quartzite claysoils Small asymmetrical crests Alto Paraguai-Guaporé Depression Vast mound-hills with flat 150 - 250 Shales Quartzarenic neosoils summits, slightly carved valleys Arkose - inconsolidated Yellow Latosoils Fluvial plains sandy sendiments

Miranda Depression Vast mound-hills with flat 150 - 200 Metasandstones, phyllite, Red-yellow claysoils summits quartzitos, limestone Not too deep valleys

On Tricart’s (1982) map, it is important to highlight Those units are denominated “pantanais” (swamps) the outline of several alluvial fans, of which the largest is due to frequent flooding by superficial waters. However, known as the Taquari Mega-fan (Figure 4). this name is inappropriate as the region does not present The plains and the Paraguay River Pantanal cover a swamps as a whole. The plains are identified according vast surface with extremely flat topography and altitudes to different genetic formation processes, such as fluvial ranging from 80 m near the Paraguay River to 150 m in plains (linked to the Paraguay River and its affluents) and higher areas. They present a complex hydrographic network fluvio-lacustrine plains (in interfluvial positions among of rivers originating from the surrounding scarps, running the rivers of the basin). through narrow alluvial plains subject to seasonal floods The flood areas are directly related to the topographic with permanent flooded areas. All rivers originating in the variations and to the kind of soil which characterises the east, northeast, south and southeast coalesce on the left behaviour of superficial and sub superficial waters. From this, riverbank of Alto Paraguay. low, average and high flood areas are known, positioned in Due to different flooding patterns these areas have been different ways in relation to the main axis of local drainage. denominated according to flood accumulation areas and The altitude varies between 150 and 180 m further from plains. These areas are traditionally known as “Pantanais the drainage axis, but areas near drainage lie at below Mato-Grossenses” or Pantanal sub-regions. 100 m altitude. This is also the case at the confluences of

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 233-240 237 Mercante, MA., Rodrigues, SC. and Ross, JLS.

Figure 4. BAP map presenting the macroforms of the relief of the surrounding plateau and the plain of the Pantanal Mato‑Grossense.

the main fluvial courses, with variable flooding periods b) cordilleras: ridges of firm terrain, locally ranging from three to four months in weak flooding areas denominated “cordilheiras”. The term up to nine months in strong flooding areas; there are also “cordilheira” is used for the innumerable marginal areas which remain flooded all year long. paleodykes or clay ridges, which are usually The flooded areas are modelled on recent sediment unflooded, ranging from one to three metres above the field levels and which cover strips of the terrain deposits along the valleys characterised by the presence (on average longer than they are wide). These are of marginal dams, sandy bars, islands and circular and preferred areas for the location of cattle ranches, semi-circular shaped lagoons. Some features in these areas and are very much used as a refuge for “swamp” are identified by the following regional names: livestock and by the regional fauna during the a) baias: small depressions in the terrain presenting flood season; different forms (circular, semicircular or irregular), c) vazantes: vast elongated depressions located which may contain water. They may or may not be between the “cordilheiras” which serve as fluvial covered by aquatic species of plants; courses up to many kilometres long and which

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may be intermittent or perennial, or may connect The fluvio-lacustrine plains correspond to the deposits bays or streams; of the marginal areas in the lagoons in the hydrodynamic d) corixos: channels with temporary or perennial processes of flooding and “vazantes” where they vary in drainage which connect adjacent baias or even the quality of the carried sediments. bigger water courses. They are more powerfully It is important to mention the hills scattered along erosive than the “vazantes” (presenting more isolated areas of the plain, which are usually round and from excavated beds which are usually narrower and 150 to 200 m high on average. During the flooding season deeper); they stand out in the flooded areas like islands covered in e) capões or caapões: islands of trees usually in an vegetation. The hills located on the west side are not part area located from 0.3 to 30 m above the field. It is of the plain, but are eroded areas of the Amolar Mountains. slightly hilly, measuring from five to one hundred metres in diameter, where the vegetation becomes 5. Final Considerations denser and the trees are from many different Despite offering generic data and being more species of flora in the savannah; classificatory for BAP units, the analysis of published f) oxbow lakes: these lakes are on the banks of many articles makes it possible, by means of the conceptions rivers and have a significant role in the freshwater adopted by their authors, to relate geomorphologic dynamics biodiversity as they are reproduction and feeding and relief forms with the biodiversity of the plain and the sites for many species. They may present high Pantanal of the Paraguay River, i.e., the Pantanal Mato- connectivity with the original system (the river) Grossense. due to the relief, distance and the magnitude of the The approach made it possible to reach some conclusions: flood rhythm. They are often known as baias; 1) The landscape of the Pantanal has become a g) fluvial avulsion: fluvial avulsion starts with the symbol for biodiversity and environmental breaking of marginal dykes and sedimentation on challenge with a double mission: to enrich the adjacent low areas which become flooded during biodiversity and not allow the degradation of Pantanal with predatory and inadequate uses; flooding seasons. The breaks in marginal dykes 2) The Pantanal is definitely a complex and are known by the communities in the Pantanal as heterogeneous space cell inland in the South “arrombados”. During the floods part of the water American continent and in order to establish starts to flow towards the flood plain through the biodiversity conservation and recovery strategies “arrombado” and the channel may split, originating the link with its geomorphology is indispensable; a distributary channel. In case the new distributary 3) The Pantanal Mato-Grossense is a natural system channel becomes the main channel, which usually which has been slightly transformed by human implies abandonment of the old channel, leading action and at the same time a fragile microcosm of to a drastic change in the river course; and rich biodiversity against the threat of turning into h) fluvial plains: These are the various strips of land an environmental system that is highly degraded where sediments accumulate. This is a result of and modified by human actions; the surface drainage difficulties along practically 4) Its geomorphologic evolution process, which all the watercourses of the Paraguay River and has been going on for thousands of years with its main tributaries which flow down the plateau a sedimentary dynamic on the alluvial fans, is towards the plain, such as the rivers Bento Gomes, continuously changing due to the alterations in Cuiabá, São Lourenço, Itiquira, Taquari, Negro, accumulation and deposit of sediments as well as Aquidauana, Miranda, Nabileque and Apa. due to the dynamics of its drainage system; and Many factors must be considered when analysing 5) Such a complex relationship on a wet area forms how exogenous processes act on the fluvial plains, in the a picture of an exceptional landscape in Brazil superficial drainage of water (speed, discharge and kinds with the recognition of its importance on the international scene. of flow), subterranean infiltration and drainage, time of residence of the water in the system, water table fluctuation, Acknowledgements – CAPES/MEC, for the support to the Project kinds of transport of the sediments (channelled or spread of Academic and Scientific Cooperation - Procad nº 067/2007; flow), deposit of sediments on the riverbed, sedimentary to the Laboratório de Geomorfologia da Universidade de São Paulo and to the Laboratório de Geomorfologia e Erosão dos processes on the flood plains, avulsion and divergence Solos (LAGES) da Universidade Federal de Uberlândia (UFU). of the channels. The processes of deposition and erosion are constant. References This is highlighted by the migration and abandonment of the beds, by the formation of marginal dykes, changes in AB’SABER, AN., 1988. O Pantanal Mato-Grossense e a teoria dos channels by avulsion processes and the breaks known as refúgios. Revista Brasileira de Geografia, vol. 50, no. 2, p. 9-57. arrombados. These processes of alterations in the landscape -, 1996. Estratégias para recuperação da biodiversidade regional. are intense in the alluvial fan of the River Taquari (Mercante In DENCKER, AFM., Org. Comunicação e meio Ambiente. São et. al., 2007). Bernardo do Campo: INTERCOM /CAPES.

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ABDON, MM., VILA da SILVA, JS., SOUZA, IM., ROMON, MERCANTE, MA. and PAIVA, LA., 2009. A institucionalização VT., RAMPAZZO, J. and FERRARI, DL., 2007. Desmatamento da interdisciplinaridade no ensino de pós-graduação e aplicações no bioma Pantanal até o ano 2002: relações com a fitofisionomia de geotecnologias no Pantanal. In Anais do II Simpósio de e limites municipais. Revista Brasileria de Cartografia. Geotecnologias no Pantanal. Corumbá, MS: Embrapa Informática Agropecuária; São José dos Campos: INPE. p. 1041-1048. ALHO, CJR., 2008. Biodiversity of the Pantanal: response to seasonal flooding regime and to environmental degradation. MERCANTE, MA. and SANTOS, ET., 2009. Avulsões no Revista Brasileira de Biologia = Brazilian Journal of Biology, Pantanal: dimensões naturais e sociais no rio Taquari. Revista vol. 68, no. 4, p. 957-966. Suppl. Sociedade & Natureza, vol. 21, no. 3, p. 361-372. ALHO, CJR. and GONÇALVES, HC., 2005. Biodiversidade MERCANTE, MA., GARNÉS, SJA., PAIVA, LA., SANTOS, ET. do Pantanal. Ecologia e conservação. Campo Grande-MS: and NOGUEIRA, AX., 2007. Alterações causadas por avulsão no rio Taquari no Pantanal Mato-Grossense. Revista RA´E GA, UNIDERP. 142 p. no. 13, p. 77-86. ASSINE, ML., 2003. Sedimentação na Bacia do Pantanal ROSS, JLS., 1990. Geomorfologia: ambiente e planejamento. Mato-Grossense, Centro-Oeste do Brasil. Rio Claro: Instituto de São Paulo Contexto. Geociências e Ciências Exatas da Universidade Estadual Paulista. 106 p. Tese de Livre Docência. -, 2006. Ecogeografia do Brasil: subsídios para planejamento ambiental. São Paulo: Oficina de Textos. ASSINE, ML., PADOVANI, CR., ZACHARIAS, AA., ANGULO, RJ. and SOUZA, MC., 2008. Compartimentação geomorfológica, ROSS, JLS., VASCONCELOS, TNN. and CASTRO-JÚNIOR, processos de avulsão fluvial e mudanças de curso do Rio Taquari, PR., 2005. Estrutura e formas de relevo. In MORENO, G. and Pantanal Mato-Grossense. Revista Brasileira de Geomorfologia, HIGA, TCS., Org. Geografia de Mato Grosso: território, sociedade, vol. 6, no. 1. ambiente. Cuiabá: Entrelinhas. p. 218-237. Conservação Internacional, 2009. Bacia do Alto Paraguai – SILVA, TC., 1984. Contribuição da geomorfologia para o Monitoramento das alterações da cobertura vegetal e uso do conhecimento e a valorização do Pantanal. In Anais do I Simpósio solo- período de 2002 a 2008. Roteiro técnico e metodológico. Sobre Recursos Naturais e Sócio-Econômicos do Pantanal. Corumbá, MS: CPAP-EMBRAPA, UFMS. p. 77-90. Available from: . Access in: 20 maio 2010. TRICART, J., 1972. La Terre Planéte Vivante. Paris: Presses FRANCO, MS. and PINHEIRO, R., 1982. Geomorfologia. In Universitaires de France, Boulevard Saint-Germain. Edit. nº. 31977. BRASIL. Projeto RADAMBRASIL: folha SE. 21: Corumbá e parte da Folha SE. 20: levantamento de recursos naturais. Rio -, 1982. El Pantanal: un ejemplo del impacto geomorfologico de Janeiro: Ministério das Minas e Energia/Secretaria Geral. sobre el ambiente. Revista Informaciones Geograficas (Chile), vol. 27, p. 161-224. vol. 29, p. 81-98.

240 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 233-240 Hydrological cycle Gonçalves, HC.a*, Mercante, MA.b* and Santos, ET.c* aAgência Nacional de Águas, SPS, Área 5, Quadra 3, Bloco B, CEP 70610-200, Brasília, DF, Brazil bPrograma de Pós-graduação em Meio Ambiente e Desenvolvimento Regional, Universidade Anhanguera – Uniderp, Rua Alexandre Herculano, 1400, Jardim Veraneio, CEP 79037-280, Campo Grande, MS, Brazil cUniversidade Anhanguera – Uniderp, Rua Ceará, 333, Miguel Couto, CEP 79003-010, Campo Grande, MS, Brazil *e-mail: [email protected], [email protected], [email protected] Received October 14, 2010 – Accepted December 13, 2010 – Distributed April 30, 2011 (With 5 figures)

Abstract The Pantanal hydrological cycle holds an important meaning in the Alto Paraguay Basin, comprising two areas with considerably diverse conditions regarding natural and water resources: the Plateau and the Plains. From the perspective of the ecosystem function, the hydrological flow in the relationship between plateau and plains is important for the creation of reproductive and feeding niches for the regional biodiversity. In general, river declivity in the plateau is 0.6 m/km while declivity on the plains varies from 0.1 to 0.3 m/km. The environment in the plains is characteristically seasonal and is home to an exuberant and abundant diversity of species, including some threatened with extinction. When the flat surface meets the plains there is a diminished water flow on the riverbeds and, during the rainy season the rivers overflow their banks, flooding the lowlands. Average annual precipitation in the Basin is 1,396 mm, ranging from 800 mm to 1,600 mm, and the heaviest rainfall occurs in the plateau region. The low drainage capacity of the rivers and lakes that shape the Pantanal, coupled with the climate in the region, produce very high evaporation: approximately 60% of all the waters coming from the plateau are lost through evaporation. The Alto Paraguay Basin, including the Pantanal, while boasting an abundant availability of water resources, also has some spots with water scarcity in some sub-basins, at different times of the year. Climate conditions alone are not enough to explain the differences observed in the Paraguay River regime and some of its tributaries. The complexity of the hydrologic regime of the Paraguay River is due to the low declivity of the lands that comprise the Mato Grosso plains and plateau (50 to 30 cm/km from east to west and 3 to 1.5 cm/km from north to south) as well as the area’s dimension, which remains periodically flooded with a large volume of water. Keywords: Pantanal of Brazil, water resources, hydrologic regime.

Ciclo hidrológico

Resumo O ciclo hidrológico do Pantanal guarda um significado importante na bacia do Alto Paraguai, a qual compreende duas áreas em condições consideravelmente diversas no que se refere aos recursos hídricos e naturais, o planalto e a planície. Sob o enfoque de função ecossistêmica, o fluxo hidrológico na relação planalto-planície é importante para a criação de nichos reprodutivos e alimentares para a biodiversidade regional. Em geral, a declividade dos rios no planalto é de 0,6 m/km enquanto que a declividade na planície é de 0,1 a 0,3 m/km, e o ambiente na planície é caracteristicamente sazonal e mantém uma diversidade de espécies exuberantes em abundância, inclusive de animais ameaçados de extinção. Ao encontrar a planície, a superfície plana faz diminuir o fluxo de água no leito dos rios e, na época de chuva, os rios transbordam seus leitos, inundando a planície. A precipitação média anual da bacia é de 1.396 mm, variando entre 800 mm e 1.600 mm, e as maiores chuvas são observadas na região do planalto. A baixa capacidade de drenagem dos rios e lagos que formam o Pantanal e o clima da região fazem com que, aproximadamente, 60% de todas as águas provenientes do planalto sejam perdidas por evaporação. A bacia do Alto Paraguai, incluindo o Pantanal, embora tenha abundante disponibilidade de recursos hídricos, apresenta situações de escassez em determinadas sub-bacias e em determinadas épocas do ano. As condições climáticas por si só não são suficientes para explicar as diferenças que são observadas no regime do rio Paraguai e de alguns de seus afluentes. A complexidade do regime hidrológico do rio Paraguai está relacionada à baixa declividade dos terrenos que integram as planícies e pantanais mato-grossenses (de 50 a 30 cm/km no sentido leste-oeste e de 3 a 1,5 cm/km de norte para o sul) e também à extensão da área que permanece periodicamente inundada com grande volume de água. Palavras-chave: Pantanal do Brasil, recursos hídricos, regime hidrológico.

The opinions expressed in the text are the sole responsibility of the authors.

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 241-253 241 Gonçalves, HC., Mercante, MA. and Santos, ET.

1. Introduction water resources: the Plateau and the Plains (Figure 1). The Plateau is located on the north and east of Alto Paraguay The Alto Paraguay Basin, covering roughly hydrographic basin. It is a relatively high altitude area, 600,000 sq km, has 362,376 km in Brazil, comprising with datum levels above 200 m, sometimes reaching 4.3% of the national territory, that basin holds considerable 1,400 m, located in the basin’s eastern region, almost importance in the strategic context of water resources entirely within Brazilian territory, where drainage is well management for Brazil, and Paraguay, which defined and converging. The Pantanal, one of the main share it not only for its dimensions, but for being home biomes in South America, is located in the lowlands, also to the Pantanal, one of the largest stretches of flooded comprising flood-prone areas in Bolivia and Paraguay. areas in the planet, with 147,574 sq km, constituting a The Pantanal is a lowland area, located in the centre link between the Cerrados in Brazil, and the Chaco in of the basin, where the rivers flood the plains and feed an Bolivia and Paraguay. intricate drainage system comprised of extensive lakes, The drastically seasonal environment of the Pantanal diverging water bodies and seasonal drainage and flooded boasts a diversity of exuberant and abundant species, areas. The Pantanal region possesses datum levels ranging including endangered species. Aspects of flooding and from 80 m to 150 m and was formed by the sinkage of a large drainage, topography and nutrients strongly influence the area, which occurred simultaneously with the emergence landscapes and the supplies of feeding and reproductive of the Andes Mountain Range (Silva, 1984). The datum niches for the native fauna. level of 200 m altitude corresponds, approximately, to the The present study, which adopts an ecosystem function boundaries of the Pantanal lowlands, and the steep slopes, focus, aims to demonstrate that the hydrologic flow of the mountains and the Plateau’s tablelands. Pantanal is related to the geographic position of the Upper Finally, there is the Chaco, located west of the Brazilian Paraguay Basin, with its plateau and plain compartments border, which is a lowland area, where precipitation is that interact to form reproductive and feeding niches for below 1,000 mm per year, with large areas where river the biodiversity of the region. flow forms swamps or lakes, which rest without a defined drainage system. 2. Procedures Adopted While the fountainheads of the rivers that form the Data were extracted from integrated management Pantanal have their origins in the highlands, with a action programmes for the Pantanal and Upper Paraguay predominant cerrado biome, and typical environmental, Basin (ANA, 2008), in which the combined strategies economic and social context of the cerrado, the flooded aim to demonstrate that the Pantanal is important for lowlands below, called Pantanal, have their own unique the management of water resources in Brazil and the characteristics of seasonably flood-prone areas. neighbouring countries that share this basin – Bolivia It must be noted, for instance, that roughly the same and Paraguay. amount of water that comes from local precipitation in In order to correlate water resources with the rich the Pantanal is lost through evapotranspiration. Thus, the biodiversity of the Pantanal, data were inserted containing regime of flooding and draining, which is fundamental for ecosystem approaches (Alho and Gonçalves, 2005). the functions of the natural system, relies fundamentally on the cerrado portion – the fountainheads on the highlands, 3. Pantanal and the Ecosystem Context a vital fraction in the BAP for the Pantanal. From the perspective of ecosystem function, the The Pantanal is a lowland area subject to periodical crucial element for the functioning of the Pantanal system flooding, which is nationally and internationally recognised in the relationship between plateau and lowlands, is the for the exuberance of its biodiversity, as a humid area of hydrologic flow that creates feeding and reproductive utmost importance in the globe. It is part of the Upper niches for the regional biodiversity. Because of those Paraguay River Basin (BAP) and is formed by the Paraguay characteristics, the Cerrados/Pantanal system is considered River and, in Brazil, by its tributaries, especially the ones one of the biodiversity and water resources hot-spots in the located on the left bank. planet, for its importance and for the degree of exposure The river Paraguay is one of the major tributaries of the to environmental threats. Prata River Basin, the second largest river basin in South The lowlands are formed by the tributaries on the left America, outsized only by the Amazon Basin, expanding bank of the Paraguay River, within Brazilian territory, with through a total area of 3,100,000 sq km, draining almost its western border touching the territory of Bolivia to the 20% of the South American continent. Of all the rivers that north and Paraguay to the south (Figure 2). form the Prata River Basin, the Paraguay River is the one The plateau’s fountainheads feed different basins, that runs deepest into the centre of the continent. Before in accordance with slope direction. The waters from the its confluence with the Paraná river, it runs an extension of highlands at the extreme northern portion of Alto Paraguay 2,612 km, 1,683 km of which is within Brazilian territory, Basin (Parecis and Cuiabá) flow toward the Amazon with some sections shared with Bolivia and Paraguay. Basin on the northernmost side, and to BAP through the The Alto Paraguay Basin comprises two areas with downward slope running towards south; the eastern slopes considerably diverse conditions regarding natural and (Bodoquena, Maracaju and São Jerônimo) drain through

242 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 241-253 Hydrological cycle

Figure 1. Location of the Pantanal/Upper Paraguay River in Brazil (ANA, 2004).

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 241-253 243 Gonçalves, HC., Mercante, MA. and Santos, ET.

Figure 2. Upper Paraguay River Basin in Brazil - Diagram f the hydrographic network (ANA, 2004).

244 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 241-253 Hydrological cycle the eastern declivity towards Araguaia and Paraná rivers, In the Pantanal, the flooding area of the alluvial fans and, through the western declivity they flow into the Alto has an average expanse of 50,000 km2 (Figure 5). Ladário is Paraguay Basin. the reference fluviometric station in the Brazilian Pantanal. The main rivers running down from the highlands The station has been monitored by the Brazilian Navy since into the plains are: from north to south, Paraguay, Bento 1900. When the maximum annual level in Ladário reaches Gomes, Cuiabá, São Lourenço - Itiquira, Taquari, Negro, or exceeds 4 m, it is considered that there is flooding in the Aquidauana - Miranda, Nabileque and Apa rivers. Pantanal; When the level varies between 4 and 5 m, the When the flat surfaces meet the plains, they slow down flood is light; between 5 and 6 m, it is considered normal the water flow in the riverbeds and during the rainy season, and above 6 m, it is deemed a severe flood. In years of the rivers overflow their banks, thus flooding the lowlands. very intense rainfall, such as 1988 (6.64 m, the greatest In general, river declivity in the plateau is 0.6 m/km historical mark) and 1995 (6.56 m, third greatest mark in while declivity on the plains varies from 0.1 to 0.3 m/km. the century), the Paraguay River, in the Pantanal, overflows The depressions get filled with water, forming the baías, its banks by flooding and expands to a width of 20 km. which are channels linking flooded valleys, shaping the Land submersion depth in the Pantanal ranges from 0.5 m channels (corixos); and shallower depressions interconnect to 1.5 m in average. Submersion duration varies greatly. the flooded areas, forming the drainage ditches. In some areas the floods may last up to six months. The The Basin does not boast a wide climate variation floods confined in the sub-basins do not have a direct and may be wholly classified as a tropical humid climate. influence on the Pantanal floods. Average annual temperatures vary between 22.5 ºC and The low drainage capacity of the rivers and lakes that 26.5 ºC. The hottest month is November (with an average form the Pantanal, coupled with the region’s climate, produce temperature of 27 ºC) and the coolest is July (with an intense evaporation. Approximately 60% of all the waters average temperature of 21 ºC). originated from the Plateau are lost through evaporation. Average annual precipitation in the Basin is 1,396 mm, The current knowledge of the conditions of the Alto ranging from 800 mm to 1,600 mm, and the heaviest Paraguay Basin, in terms of surface water availability and rainfall occurs in the Plateau region. The rainy season is demand, indicates that the greatest demand in the entire from October through April and the other months make up Pantanal/Alto Paraguay Basin is destined to animal drinking. the dry season. Average annual evaporation is 1,239 mm, The greatest demands for irrigation are located in areas of with peaks in August, when higher rates of insolation are the Miranda, Itiquira and Correntes rivers sub-basins. The observed (Figure 3). greatest urban and industrial demands are located in the The average water flow in the Basin was 2,464 m3/s, at Alto and Médio Cuiabá river basins. Those demands are the confluence with the Apa river, in the period 1939‑2002 relatively small (3.5%) as compared to the average water (Figure 4). The Pantanal acts as a great reservoir, retaining availability. It should be noted, however, that urban and the largest share of the waters originated from the Plateau, rural water supply in the Pantanal/Alto Paraguay Basin thus regularising the flow from Paraguay River during up makes widespread use of water collection from shallow to five months, between inflows and outflows. In Cáceres, and deep wells. the greatest average flow happens in March, at the end of The Alto Paraguay Basin, including Pantanal, while the rainy season; in Porto São Francisco, it occurs in April boasting an abundant availability of water resources, also and May; in Porto Murtinho the flow is greater in June and presents some conditions of scarcity in some sub-basins July, entirely outside the rainy season. In the Plateau, the and different periods of the year, due to the hydric balance specific flows reach 13/18 l/s/ sq km and, in the Pantanal, or the observed use. in general, they are less than 0.5 l/s/sq km. Table 1 shows The rivers in the region have the capacity to convey the average monthly and annual flow in the Pantanal and the average discharges, but during the flood season, they Alto Paraguay Basin (ANA, 2004). inundate extensive areas of lowlands, forming temporary On the northern portion of the Pantanal, the relative lakes that take up a total area of roughly 100,000 sq km. contribution of the tributaries coming down from the plateau In early May, the water level starts to slowly go down, accounts for 72% of the flows running into the Paraguay and the area becomes characteristically swampy. When River. For the southern Pantanal, it corresponds to 28%. the lowlands dry up, the soils are covered with a thin layer The northern portion of the Pantanal receives of nutrients that fertilise the that feed a herd contributions from: Alto Paraguay - 27%; Alto and estimated in three million heads. Médio Cuiabá - 20%; São Lourenço - 14%; Correntes- As for underground waters, the basin’s largest portion is Itiquira-Piquiri - 11%. made up of porous aquifers associated with non consolidated The contributions in the southern portion of the sediments that cover ancient rocky substratum. The Pantanal come from: Alto Taquari - 16%; Negro - 3%; underground aquifers are located at an average depth of 50 m Alto Aquidauana - 5% and Alto Miranda - 4%. It should be and their discharge exceeds an average of 30,000 L/h. there noted that the Basin’s declivity in the plateau is 30 cm/km is an abundance of underground water in the Pantanal, but on average, and in the Pantanal it is 3-5 cm/km, running there is some evidence of potential forthcoming problems from east to west and 1.5 to 3 cm/km in the north-south with water quality, in terms of salinity and the presence direction, towards the Paraguay River. of heavy metals. In general terms, the quality of water

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 241-253 245 Gonçalves, HC., Mercante, MA. and Santos, ET.

Figure 3. Upper Paraguay River Basin in Brazil – Average monthly and annual rainfall (ANA, 2004).

246 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 241-253 Hydrological cycle

Figure 4. Upper Paraguay River Basin in Brazil - Average Monthly and Annual Flows (ANA, 2004).

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 241-253 247 Gonçalves, HC., Mercante, MA. and Santos, ET. 2003 2003 2002 2002 2003 2002 1981 2003 2003 2003 2003 2003 1993 1965/ 1967/ 1962/ 1966/ 1965/ 1969/ 1969/ 1969/ 1967/ 1967/ 1967/ 1966/ 1968/ period Observation Observation /s) 3 (m 95 64 84 35 537 180 590 229 359 388 140 317 117 254 101 698 321 638 320 142 245 128 73.5 26.2 76.2 45.2 1,492 flow Q flow Annual average Annual average D 86 521 590 464 521 217 407 525 659 940 373 261 82.9 N 65 343 447 246 262 119 260 188 537 940 316 250 78.3 O 279 367 158 178 188 163 456 278 241 84.6 51.9 69.8 1,028 S 262 348 114 142 165 152 425 248 225 68.7 45.6 67.5 1,198 /s 3 A 6.3 268 365 107 132 155 154 459 238 229 43.6 65.9 1,420 J 314 439 124 144 180 178 567 248 239 70.1 49.2 69.2 1,708 J 400 558 155 199 227 210 731 267 248 84.3 57.1 74.1 1,991 M 565 714 243 382 112 301 261 876 294 258 68.6 79.6 2,229 Average monthly flows in m monthly flows Average A 799 831 451 596 190 441 354 961 343 269 84.3 88.7 2,267 M 869 745 832 279 571 110 422 974 433 280 98.1 1.010 1,950 F 932 830 808 810 317 550 113 400 936 479 279 97.6 1,335 J 753 738 698 717 287 517 104 351 811 438 271 92.7 1,048 5,100 3,030 32,774 48,360 23,226 27,050 11,995 21,800 17,150 27,040 32,285 102,750 243,000 66070004 66090000 66260001 66280000 66450001 66460000 66525000 66490000 66600000 66750000 66810000 66870000 66885000 Code and area (sq km) area River and River station name Paraguay Cáceres Source: ANA (2004). Paraguay Descalvos Cuiabá Cuiabá Cuiabá Barão de Melgaço Vermelho Rondonópolis São Lourenço Córrego Grande Itiquira Estrada BR-163 Correntes Estrada BR-163 Piquiri São Jerônimo Cuiabá Porto Alegre Paraguay São Francisco Taquari Coxim Taquari Porto Rolom Table 1. Pantanal and Alto Paraguay Basin average monthly annual flows. Table

248 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 241-253 Hydrological cycle 2003 1986 2003 2003 1981 2002 2002 1969/ 1968/ 1968/ 1965/ 1963/ 1939/ 1971/ period Observation Observation /s) 3 (m 95 2.8 4.8 815 116 903 50.6 32.3 87.6 16.7 81.3 1,892 1,889 1,053 2,376 flow Q flow Annual average Annual average D 162 134 153 76,1 1,332 1,290 1,701 N 38 112 101 87.9 1,312 1,327 1,776 O 23 85.1 63.4 57.3 1,500 1,538 2,145 S 12.6 66.2 46.1 40.4 1,772 1,768 2,566 /s 3 A 16.2 59.1 40.2 39.2 2,027 1,982 2,871 J 47 32.6 66.4 37.3 2,222 2,246 2,999 J 57.4 86.7 76.8 77.5 2,363 2,402 2,989 M 110 66.5 80.5 88.7 2.331 2,438 2,818 Average monthly flows in m monthly flows Average A 117 80,3 90.4 73.6 2.210 2,345 2,506 M 121 164 118 90.8 1.927 2,053 2,266 F 119 178 144 102 1.716 1,792 2,008 J 129 188 155 128 1.502 1,485 1,827 14,770 15,200 15,460 11,100 316,000 363,500 474,500 66895000 66890000 66945000 66910000 66960008 67100000 67170000 Code and area (sq km) area River and River

station name Paraguay Porto da Manga Source: ANA (2004). Negro Fazenda Rio Negro Aquidauana Aquidauana Miranda Miranda Paraguay Porto Esperança Paraguay Porto Murtinho Apa São Carlos Table1. Continued... Table1.

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 241-253 249 Gonçalves, HC., Mercante, MA. and Santos, ET.

Figure 5. Upper Paraguay River Basin in Brazil – Areas susceptible to fl ooding (ANA, 2004).

250 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 241-253 Hydrological cycle in the plateau may be considered good, although water Murtinho is 2,376 m3/s-1, other estimates show a discharge availability is somewhat more restricted to some areas. of 2,500 m3/s-1 in Corumbá (Hamilton et al., 1997). The Pantanal regulates river discharge through periodical Hydrologic data show that there are marked differences flooding. It hoards the waters and also stimulates water loss between the northern and southern portions of Pantanal: through evapotranspiration and soil infiltration. The river the flood regime and flood fluctuation is greater in the sediments are retained during the passage of river waters north. However, the physical and chemical conditions through the Pantanal with the consequent transformation of of the waters in the southern portion of the Pantanal are solutions and biogeochemical elements that are important more stable than in the northern portion, since the north is for the biodiversity in the region. drier in the dry season. Peak discharge from the tributaries occurs earlier than the Paraguay River discharge, and 4. The Natural System and its Functioning the subsequent elevation of the Paraguay River waters block the flow of its tributaries (Hamilton et al., 1996). 4.1. Dynamics of inundation As mentioned before, the flood peaks produced by the Paraguay River discharge in the south occurs four months Hydrology in the Pantanal is irregular: even being later than rainfall peaks in the riverheads, so the floods seasonal, the flood periods vary throughout the plains, due are mainly caused by river overflow and not by rainfall to the volume of water flows running into the lowlands and (Hamilton et al., 1996). to the smooth and flat declivity of the terrain. The flood The largest flood-prone areas are located along the periods may be delayed after rainfall on the riverheads in Paraguay River, between Porto Conceição and Porto the plateau, due to the slow passage of the waters through Murtinho, reaching depths of 1 m to 1.5 m. Those floods the flooded plains. A great portion of the Pantanal is flooded may last for up to six months. In the other areas of the by river discharge, which overflows their banks when Pantanal, submersion of the flood-prone areas has a depth they reach the Pantanal, but in some specific spots, the of roughly half a metre and the flood duration varies from local rainfall may also produce shallow floods. During the region to region. In the area of Paraguay and Jauru rivers, period of high water levels, the water flows move slowly it lasts approximately 70 days; in Cuiabá, Aquidauana- through the Pantanal, interconnecting the rivers with the Miranda, it lasts roughly 40 days and in Taquari and São depressions, through canals and drainage ditches, filling Lourenço rivers, the duration is about 30 days, according up the flood-prone areas. The water level at the Paraguay to data from PCBAP (1997a). In the portion of Pantanal River channel in Ladário is close to 6 m and approximately that receives water from the Negro and Taboco rivers, the 2 m in the portion where the river overflows in the plains. flood may reach 1.2 m and last up to 90 days. The flood- The Paraguay River runs from north to south along prone area measures approximately 300 km by 400 km, and the western part of Pantanal, and receives water from its may reach a total area of approximately 137,000 sq km, tributaries, particularly the ones located on the left bank. mostly within Brazilian territory and some small sections River declivity in the Pantanal is 2.5 cm per km (EDIBAP, in Bolivia and Paraguay (Hamilton et al., 1996, 1997). 1979) and there is the presence of large lakes along the Long-range studies show that the flood pattern in river, with close hydrologic relationship with the Paraguay the Pantanal varies from February, in the north, through River, which has a sinuous shape in the Pantanal portion. June, in the south, as a result of the drainage delay in the Those lakes are: to the south of Corumbá, Jacadigo Lake; region (Hamilton et al., 1996, 1997). During nine years to the north of Corumbá, we find Baía Vermelha, Lagoa of observations, an area of 131,000 sq km was flooded, Mandioré, Lagoa Guaíba and Lagoa Uberaba. Past the between 1979 and 1987. The estimates for total monthly city of Cáceres, the river declivity ranges from 6.3 cm flooded areas vary between 11,000 and 110,000 sq km. km-1 to 1 cm km-1 near the Apa River (Carvalho, 1986). After receiving a strong influx of water in its riverheads, 4.2. Seasonality and yearly cycles the Paraguay River supplies water to the flood-prone areas There are very pronounced seasonal floods in the of the Pantanal, but the flood wave may be delayed by alluviums of Taquari, with peaks occurring in February. four to five months until it reaches the southern portion This demonstrates the inter-annual variability in maximum of Pantanal. Thus, the changes in water levels show that and minimal levels of the flooded areas (Hamilton et al., there is a delay of approximately four months before 1998). The water influx from the river Taquari has its the water level passes through the Pantanal, from north peak one or two months after rainfall peak in the region. to south, and reaches the city of Corumbá. During this Thus, the floods may be a result of that influx and also of period, when water levels reach their peak in Corumbá, the local rainfall. After March, the water deficit is explained dry season is already underway in the northern Pantanal by the evapotranspiration of the flooded area. (Hamilton et al., 1996). The areas where the Taquari river fountainheads are In the city of Corumbá, the Paraguay River annual located have an erosive potential, but are protected by natural discharge is 1,260 m3/s-1 (cubic metres per second) plant cover. With the advent of deforestation, the erosion when the river accounts for 80% of the flow in the region became more severe, producing the so-called arrombados (EDIBAP, 1979). While the National Water Agency (ANA, of the Taquari River in the Pantanal. Arrombados are 2004) estimates that the Paraguay River discharge in Porto fissures in the river bank caused by intense siltage in the

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 241-253 251 Gonçalves, HC., Mercante, MA. and Santos, ET. riverbed. Such alteration has provoked changes in the The Paraguay River’s fountainheads are located in seasonal flooding regime and transformed areas that were the complex of the Parecis Mountain Range, close to the only periodically flooded in areas of permanent inundation, city of Diamantino in the state of Mato Grosso. It drains currently estimated to occupy an area of 11,000 sq km the Pantanal, together with its tributaries. In the BAP, (ANA, 2004). Paraguay River expands and forms a damming zone, and In northern Pantanal, the floods occur between March becomes the main tributary of BAP, that comprises two and April, while in the south they take place from July to distinct regions: the Plateau and Pantanal. August. Between November and March there is intense Valverde (1972) considers three factors as preponderant water loss due to evapotranspiration. The heaviest rainfall for the regularity of the Paraguay river’s fluvial regime: occurs from October through March. The river flows (m3s-1) periodic annual rainfall with maximum regularity, falling on have their influx from January through April, with peaks the basin, especially on the upstream tributaries; extensive in March and the discharges occur from April through flooded and damming zone in the Pantanal, which feeds October, with peaks in June-July, measured in Porto the system during the dry season and smooth slopes in Esperança, on the Paraguay River (Hamilton et al., 1997). the longitudinal section and a great uniformity in the Maximum seasonal flood in the region occurs between gradient, from São Luis de Cáceres up until the mouth of February and April, and declines, with peak dry weather the Paraguay River. between October and December. Besides the annual Those considerations are evidence of the conjugated floods, there are variations in longer periods of time, with action of several factors in the hydrologic behaviour of no defined pattern. Such floods are influenced by several the water bodies. factors, in both the macro and micro scales. The river The upstream course of the Paraguay River in the Plateau level variations rely fundamentally on the precipitation corresponds to the fountainhead area, or mountains and characteristics each year. The river level is an indicator depressions, and because of that, the river has rapids and a declivity equivalent to 75 cm/km. One may observe that of two important variables: drainage and size of the river the riverheads have a quick response to precipitation, with canal, including the adjacent area. peak flows in the rainy season. In the plains and Pantanal, The slow flow of waters in the Pantanal is a determinant however, the average annual flow peaks occur in the dry factor for the loss of sediments in suspension, and contributes period. This is due to the basin’s characteristics, which to the drop of dissolved oxygen levels and decreased pH. has an intricate drainage system, with large flood-prone Statistical treatment of data from the hydrometric areas that act as reservoirs. station in Ladário, in the period 1900-1996, identified Thus, the Paraguay River presents a typical regime seven categories of floods, in an attempt to establish a of single mode tropical inundation in the portion where methodology for a system of flood alert (Adamoli, 1996). the Ladário station is located (Catella, 2001; Soares et al., During that period, the critical level of four metres of river 2008) or else, each year the river level in Ladário (MS), depth was exceeded in 61 out of the 97 years of observation presents one single phase of ascent (growth), reaching the recorded in Ladário. In some years, there were severe peak of flooding, and a single phase of descent (recession), floods, when the water level exceeded 6 metres (in the years not considering the little “bursts” that occur in the low 1905, 1913, 1920, 1921, 1980, 1981, 1983, 1986, 1989, water season (Galdino and Clarke, 1995, 1997). and 1995). In contrast, there were dry years, with river The phase of rising waters is called inundation and the levels below two metres (1910, 1911, 1915, 1938, 1939, lowering of waters is called leaking. Transitions between 1941, 1944, 1948 and from 1964 to 1973). In the period periods are called floods, when the river reaches its peak 1961 to 1973 there was diminished precipitation, and the level, and drought when it reaches minimum level. With extent of variations in the Paraguay River also declined, those figures in hand it is possible to characterise a period as detected by different methods (Sá et al., 1998). From as either dry or flooded in Pantanal (ANA, 2008). then on, there was a considerably more humid period, In 2006, Ladário station registered a level of 5.40 m, from 1974 to 1996. and it was considered by Soares et al. (2008) as the highest Such hydrologic seasonability, with an annual hydraulic flood peak since 1997. According to the authors, in the same pattern, is ecologically decisive for wildlife survival in year, during the phase of drying up, the levels observed Pantanal. were above the historical average, and the minimum datum attained (2.16 m in 6 December 2006) was also 5. Hydrologic Behaviour the highest since 1992. However, in spite of the large volume of water hoarded The data obtained from Ladário measurements are up in the surface or underground reservoirs of the Pantanal fundamental if one needs to get a full grasp of the hydrologic in the floods of 2006 and 2007 (Soares et al., 2008), the behaviour of the Paraguay River in the BAP section. That Ladário station registered, during the outflow of 2007, one fluviometric station possesses a vast series of levels. of the lowest minimum levels of the last 34 years, that is Moreover, the station controls approximately 81% of 88 cm on 3 November 2007. the average water outflow from the Brazilian territory In accordance with the classification by Galdino et al. (ANA, 2008). (2002), the flood in the hydrologic period 2007-2008,

252 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 241-253 Hydrological cycle as well as the floods of the two previous years, may be GALDINO, S. and CLARKE, RT., 1995. Levantamento e considered “normal”, that is, when the maximum water estatística descritiva dos níveis hidrométricos do rio Paraguai level in Paraguay River ranges between 5.00 and 5.99 m em Ladário, MS – Pantanal. Corumbá, MS: EMBRAPA-CPAP. 72 p. Documentos, 14. in Ladário. According to a bulletin from the National Water Agency -, 1997. Probabilidade de ocorrência de cheia no rio Paraguai (ANA, 2008), in early 2008 the pluviometric precipitations em Ladário, MS – Pantanal. Período 1900-1994. Corumbá, MS: were above the historical average in practically the entire EMBRAPA-CPAP. 58 p. Circular Técnica, 23. BAP. GALDINO, S., VIEIRA, LM., OLIVEIRA, H. and CARDOSO, Total rainfall in January and February exceeded the EL., 2002. Impactos da agropecuária nos planaltos sobre o historical average in 40% and 60%, respectively. The regime hidrológico do Pantanal. Corumbá: EMBRAPACPAP. increased local rainfall contributed to a quick rise of the 6 p. Circular Técnica, 37. Available from: . Access in: nov. 2009. of 2007 and beginning of 2008). HAMILTON, SK., SIPPEL, SJ. and MELACK, JM., 1996. Climate conditions on their own are not sufficient to Inundation patterns in the Pantanal wetland of South America explain the differences observed in the Paraguay River determined from passive-microwave remote sensing. Archiv fur regime and some of its tributaries. The complexity of the Hydrobiologie, vol. 137, no. 1, p. 1-23. hydrologic regime of the Paraguay River are related to the HAMILTON, SK., SIPPEL, SJ., CALHEIROS, DF. and MELACK, smooth declivity of the terrain comprised by the lowlands JM., 1997. An anoxic event and other biogeochemical effects and marshlands in Mato Grosso (between 50 and 30 cm/km of the Pantanal wetland on the Paraguay River. Limnology and in the east-west direction and 3 to 1.5 cm/km from north Oceanography, vol. 42, no. 2, p. 257-272. to south). It is also owed to the area’s extension, which HAMILTON, SK., SOUZA, OC. and COUTINHO, ME., 1998. remains periodically flooded, with a great volume of water. Dynamics of floodplain inundation in the alluvial fan of the The river’s sinuous course and the numerous geographic taquari River (Pantanal, Brazil). Verhandlungender Internationale features outcropping in the flooded plains contribute to Vereinigung fur Theoretiche und Angewandtle Limnologie, vol. 26, p. 916-922. the sluggishness of water flows. Plano de Conservação da Bacia do Alto Paraguai – PCBAP, References 1997a. Metodologia do plano de conservação para a Bacia do Alto Paraguai. Brasília: Ministério do Meio Ambiente, Programa Nacional do Meio Ambiente. vol. 1. ADAMOLI, J., 1996. Previsão de médio prazo dos níveis do Rio Paraguai em Ladário, MS. In Anais do II Simpósio sobre -, 1997b. Diagnóstico ambiental da Bacia do Alto Paraguai; Recursos Naturais e Sócio-Econômicos do Pantanal. Corumbá, t. 1 – Meio físico; t. 2 – Hidrossedimentologia; t.3 – Meio biótico; MS: CPAP-EMBRAPA, UFMS. p. 59-72. t. 4 – Sócio-economia de Mato Grosso; t. 5 – Sócio-economia de Mato Grosso do Sul; t. 6 – Aspectos hurídicos e institucionais de Agência Nacional de Águas – ANA, 2004. Strategic action Mato Grosso; t. 7 – Aspectos jurídicos e institucionais de Mato program for the integrated management of the Pantanal and the Grosso do Sul. Brasília: Ministério do Meio Ambiente, Programa Upper Paraguay River Basin. Brasília, DF: ANA/GEF/PNUMA/ Nacional do Meio Ambiente. vol. 2. OEA. 315 p. -, 1997c. Análise integrada e prognóstico da Bacia do Alto -, 2008. Boletim de monitoramento da Bacia do Alto Paraguai. Paraguai. Brasília: Ministério do Meio Ambiente, Programa Brasília, DF: ANA. vol. 3, no. 3, 21 p. Available from: Nacional do Meio Ambiente. vol. 3. . Access in: nov. 2009. de Moelet aplicada ao estudo da variabilidade do nível do rio Paraguai em Ladário, MS. Pesquisa Agropecuária Brasileira, ALHO, CJR. and GONÇALVES, HC., 2005. Biodiversidade do vol. 33, no. especial, p. 1775-1785. Pantanal. Ecologia e conservação. Campo Grande-MS: Editora UNIDERP. 142 p. SILVA, TC., 1984. Contribuição da geomorfologia para o conhecimento e valorização do Pantanal. In Anais I Simpósio CARVALHO, NO., 1986. Hidrologia da Bacia do Alto Paraguai. In sobre Recursos Naturais e Sócio Econômicos do Pantanal. Anais do I Simpósio sobre Recursos Naturais e Sócio-Econômicos Corumbá. p. 77-90. do Pantanal. Brasília, DF: EMBRAPA. p. 43-50. SOARES, MTS., SORIANO, BMA., SANTOS, SA., ABREU, CATELLA, AC., 2001. A pesca no pantanal de Mato Grosso do UGP., BERGIER, I. and PELLEGRIN, LA. 2008. Monitoramento Sul, Brasil: descrição, nível de exploração e manejo (1994–1999). do comportamento do rio Paraguai no Pantanal Sul-Mato- Manaus: Universidade do Amazonas; Instituto Nacional de Grossense – 2007/2008. Corumbá, MS: Embrapa Pantanal. 5 p. Pesquisas da Amazônia. Tese de doutorado em ciências biológicas, Comunicado Técnico, 72. Available from: . Access in: 10 mar. 2008. Estudo de Desenvolvimento Integrado da Bacia do Alto Paraguai – EDIBAP, 1979. Relatório da primeira fase: descrição física e VALVERDE, O., 1972. Fundamentos geográficos do planejamento recursos naturais. Brasília, DF: Superintendência do Desenvolvimento rural do município de Corumbá. Revista Brasileira de Geografia, da Região Centro-Oeste. vol. 34, no. 1, p. 49-144.

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Aquatic macrophyte diversity of the Pantanal wetland and upper basin Pott, VJ.a*, Pott, A.a, Lima, LCP.b, Moreira, SN.a and Oliveira, AKM.c aPrograma de Pós-graduação em Biologia Vegetal, Departamento de Biologia, Universidade Federal de Mato Grosso do Sul – UFMS, CP 549, CEP 79070-900, Campo Grande, MS, Brazil bPrograma de Pós-graduação em Botânica, Universidade Estadual de Feira de Santana – UEFS, Av. Transnordestina, s/n, CEP 44036-900, Feira de Santana, BA, Brazil cPrograma de Pós-graduação em Meio Ambiente e Desenvolvimento Regional, Universidade Anhanguera – Uniderp, Rua Alexandre Herculano, 1400, Jardim Veraneio, CEP 79037-280, Campo Grande, MS, Brazil *e-mail: [email protected] Received October 14, 2010 – Accepted December 13, 2010 – Distributed April 30, 2011 (With 1 figure)

Abstract This is a short review of the state of the art concerning diversity of aquatic macrophytes and the main aquatic vegetation types in the Brazilian Pantanal wetland and upper watershed. There are ca. 280 species of aquatic macrophytes on the Pantanal floodplain, with scarce endemism. On the upper watershed, Cerrado wetlands (veredas) and limestone springs have a distinct flora from the Pantanal, with twice the species richness. As a representative case of aquatic habitats influenced by river flood, some primary data are presented for the Pantanal Matogrossense National Park and associated Acurizal Preserve, analysing the floristic similarity among aquatic vegetation types. We comment on problems of conservation and observe that Panicum elephantipes Nees is one of the few natives to compete with the invasive Urochloa arrecta (Hack. ex T. Durand & Schinz) Morrone & Zuloaga. Keywords: flora, aquatic plants, floodplain, savanna, vereda.

Diversidade de macrófitas aquáticas do Pantanal e alta bacia

Resumo Esta é uma breve revisão sobre o estado do conhecimento sobre as macrófitas aquáticas e os principais tipos de vegetação do Pantanal brasileiro e da alta bacia. A flora da planície inundável é de aproximadamente 280 espécies, com escasso endemismo. Na alta bacia, as áreas úmidas do Cerrado (veredas) e nascentes em calcário têm flora distinta do Pantanal, com o dobro da riqueza de espécies. Como um caso representativo de ambientes aquáticos influenciados por inundação fluvial, são apresentados alguns dados primários do Parque Nacional do Pantanal mato-grossense e da Reserva Acurizal associada, analisando-se a similaridade florística entre tipos de vegetação aquática e comentando- se os problemas de conservação na região, onde foi observado que a espécie Panicum elephantipes Nees é uma das poucas nativas que competem com a invasora Urochloa arrecta (Hack. ex T. Durand & Schinz) Morrone & Zuloaga. Palavras-chave: flora, plantas aquáticas, campo úmido, savana, vereda.

1. Introduction The first botanical reports on aquatic plants of the on the regional flora (e.g. Pott and Pott, 1994, 1997). Pantanal come from European naturalists who crossed Various surveys on aquatic macrophytes of the sandy the region, as summarised by Sampaio (1916). Foremost Pantanal, flooded by rain, have been previously reported among Brazilian botanists was the pioneering Hoehne (e.g., Pott et al., 1999). Some as yet unpublished data on (1923), who collected in the Pantanal, looking closely the Pantanal Matogrossense National Park are presented, at aquatic plants, many of them mentioned in his book gathered by the authors and extracted from the Rapid (Hoehne, 1948). Ecological Assessment-Botany report (Pott et al., 2001), Then a gap occurred up until the last two decades, as a representative case of aquatic vegetation influenced when local botanists started to give some information by river flood.

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2. Results and Discussion wetlands in the headwaters and along cerrado streams of the upper basin is quite distinct from this palm formation 2.1. Flora on the plain (Pott, 2008), where it only occurs along a few Diversity of aquatic macrophytes in the Pantanal rivers (Aquidauana and Taquari) (Silva et al., 2000) and varies from the smallest ( brasiliensis Wedd.) to the is associated with species of seasonally flooded largest hydrophyte, Victoria amazonica (Poepp.) Sowerby. or riparian scrub quite different from veredas. There are at least 280 species of aquatic macrophytes Often there are large areas with assemblages dominated in the Pantanal (Pott, 2008), most of them shown in the by a single macrophyte, such as species of Oryza and identification manual by Pott and Pott (2000), considering Polygonum, generally with strong vegetative propagation, various degrees of dependence on water. The most numerous or various communities may occur within a short distance. families are (26), (19), Fabaceae Some hydrophytes survive the dry season as dormant (15), (15) and Pontederiaceae (12), and the rhizomes, which is the case of Echinodorus spp., Eleocharis best represented genera are (15), Bacopa (12), spp., Nymphaea spp., Sagittaria spp.. These are therefore Utricularia (11), Nymphaea (7), and Polygonum (7) (Pott among the first to reappear in the wet season, while others and Pott, 2000; Pott, 2008). grow from seeds (Ludwigia spp.) and spores (Salvinia), Taxonomic work on aquatic plants in the Pantanal is and many use both vegetative and reproductive strategies. as yet restricted to a few groups, such as Nymphaeaceae Year-round water level may vary up to 7 m in the river (Pott, 1998), -Lemnoideae (Pott and Cervi, 1999), system, while fluctuation is much less in non-coalescent Aeschynomene (Lima et al., 2006), and some genera have isolated ponds and most areas flooded only by rain. Flood been reviewed on a Brazilian scale, such as Panicum cycles can be drawn from daily records taken by the Navy (Guglieri and Longhi-Wagner, 2004). World-wide reviews since 1900 at the hydrometric station at Ladário. such as Utricularia by Taylor (1989) are also very useful. Some species are associated with lotic habitats, such Research on macrophyte vegetation has been carried as Ludwigia inclinata (L. f.) P.H. Raven, Nymphaea out mainly in floristics. It is often concentrated on a oxypetala Planch., but more often with lentic environments, few spots, e.g., Pott et al. (1989, 1999) at Nhumirim while some occur in both, like Eichhornia azurea (Sw.) ranch (Nhecolândia), Costa (2004) at Santa Emília ranch Kunth. Most sub-regions do not have lakes and ponds, and (Aquidauana), Nunes da Cunha et al. (2000) at Pirizal therefore have quite a monotonous landscape, compared (Poconé) and other areas of Poconé (Prado et al., 1994; to Nhecolândia, Rio Negro (part of Aquidauana) and Schessl, 1999). Abobral, which present high diversity of habitats, such Cerrado wetlands (veredas) on the upper watershed as brackish and fresh water ponds, seasonal streams, and close by headwaters of the Paraná basin have a richer floodplain channels and ancient river beds (“corixos”) flora, with at least 574 species (Pott, 2008), twice the species and anabranches. Brackish ponds (“salinas”) are poor in richness found in the Pantanal. The flora of limestone macrophyte species, where only Paspalum vaginatum Sw. springs on the Bodoquena upland is not very diverse but and charophytes occur. Along the Serra do Amolar there forms attractive underwater gardens (Pott, 1999). are large lakes (Vermelha, Uberaba, Mandioré, Gaíva, Many aquatic plants which occur in the Pantanal are etc.), with aquatic vegetation restricted to shores and elements of wide distribution, in common with wetlands wind-sheltered inlets. in other neotropical phytogeographic provinces, such as 2.1.1. Endemic and rare species Amazonia and the Paraná basin. Veredas contain many additional Poaceae, Cyperaceae, Melastomataceae, etc., The Pantanal is a Quaternary floodplain, geologically in common with other wet grasslands of South America. recent (Holocene), so very few endemic species occur, none There are floristic dissimilarities between the plain of them aquatic. However, the endemic peanut Arachis and the upper watershed (Pott, 2008), for example, in the vallsii Krapov. & W.C. Greg. can be considered aquatic, crystalline streams of Bonito (Bodoquena range) grows as it grows in 40 cm flooded mud under Copernicia alba Potamogeton illinoensis Morong (Pott, 1999), not yet found Morong, on the floodplain of Lake Baía Negra and in a few in the Pantanal, whereas the giant waterlily V. amazonica other clayey spots, where it flowers and sets fruit, with the has exclusive occurrence in oxbow lakes of the lower advantage of its long hollow peg and stem, characteristic floodplain (Pott, 2008). Also unique in Mato Grosso do structures of aquatics. A few species are quite rare or show Sul is the wetland sawgrass Cladium jamaicense Crantz very restricted occurrence, such as Nymphaea belophylla (Pott, 2008), with Chara rusbyana M. Howe covering Trickett, Eichhornia diversifolia (Vahl) Urb., Oryza gaps, on organic soil upon sedimentary calcium carbonate. grandiglumis (Döll) Prod., found near the Paraguay River However, floristic similarity of the Pantanal with wet in Cáceres, Discolobium psoraleaefolium Benth., collected grasslands of the upper basin increases towards the Cerrado only on the eastern part of the alluvial fan of the Taquari uplands, on the eastern sandy soil, with species in common River. For instance, Eulophia alta (L.) Fawc. & Rendl. such as Drosera sessilifolia A. St.-Hil., Echinodorus has been found on an old floating island, Xanthosoma grandiflorus (Cham. & Schltdl.) Micheli, Xanthosoma aristiguietae (Bunting) M. Madison, on the margins of striatipes (Kunth & Bouché) Mad., etc. Nevertheless, the the Miranda River to where rooting stems could have grass‑sedge community of Mauritia (M. flexuosa L. f.) palm been carried in pre-Columbian times as a medicinal plant.

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2.2. Life forms and cat-tail Typha domingensis Pers. (“taboal”), growing Aquatic macrophytes have been grouped according in swampy areas or temporary ponds. Cat-tail tends to to their life form, into submerged, free floating, rooted increase in disturbed flooded areas and artificial ponds floating, emergent and amphibious (Irgang et al., 1984), (borrow pits and dredged water holes for cattle), while and epiphyte (Tur, 1972). Usually life form zoning occurs Rhynchospora trispicata (Nees) Steud. and Scleria variegata according to water depth: amphibians on the littoral, (Nees) Steud. are very frequently found. emergents on the shallow belts, and others in the deeper 2.4. Annual cycle zones (Pott et al., 1989). Aquatic plants respond well to the flood dynamics. 2.3. Types of aquatic habitats and main vegetation types Many shallowly flooded grasslands dry up and the According to Silva et al. (2007), there is a total of seasonal aquatics disappear, among them even perennials, 2,557 km2 of open water in the dry season of the Pantanal, such as Pontederia parviflora Alexander and Sagittaria considering only that with a vegetation-free surface. However, guayanensis Kunth, as do small annuals like Bacopa spp. the flooded area varies from 7 to 70% of the Pantanal, and Echinodorus tenellus (Mart.) Buch. A difference is so at high flood it may reach 110,000 km2, according to that in the Pantanal there is a stronger wet and dry cycle, Hamilton et al. (1996), who used radar images, so also whereas on the upper watershed the flood pulse is much taking into account floating aquatics. lower, even where there is 50-100% more rainfall. Here Floating mats (“camalote”) and floating meadows soils remain waterlogged or with a high water table all (“baceiro”, “batume”) are both found in permanent water year round, fed by ground water in the dry season, flowing bodies such as ponds, lakes, canals, oxbows and rivers. The over an impermeable layer of laterite, making the water floating aquatic “batume” was defined by Da Silva (1984). ferruginous, or over basalt or sandstone. Plant distribution Floating mats are attached banks of floating macrophytes, in cerrado wet grassland and vereda is related to ground- or they may not be anchored, so that they float downriver water level (Meirelles et al., 2002), yet in the Pantanal the or may be driven by wind; the main species of these are water table may fall below 2 m in the dry season, hence the water hyacinths Eichhornia crassipes (Mart.) Solms above-ground water level in the wet is a more important and E. azurea (Sw.) Kunth, then both can be uprooted and factor. In parts of the Pantanal, these changes in the dry become free-floating. On top of them and on free-floating and aquatic phases are more pronounced, reflected in a aquatic plants (water lettuce, Pistia stratiotes L., water high proportion of opportunistic therophytes (Schessl, fern Salvinia auriculata Aubl.), Oxycaryum cubense 1999), on intermediate ground between floodless and (Poepp. & Kunth) Palla starts to grow, with densely deep flooded stretches. Vereda soils are more organic and entangled long hollow roots and rhizomes, and gradually peaty, acting like a water storing sponge. These soils are the floating mats become floating meadows, with denser organosoils and gleysoils (Ramos et al., 2006). The soils vegetation, made up mainly of Eleocharis plicarhachis in the Pantanal, even though hydromorphic too, vary from (Griseb.) Svenson, rooted on histosol, as long as the pond pure sand to heavy clay, but due to the very flat landscape, does not dry (Pivari et al., 2008). Histosol is a sort of in the dry period the water table reaches the surface only in organic soil made of decomposing plants (Neiff, 1978). depressed parts, for example in ponds and water courses. As the floating meadow ages, the histosol thickens up 2.5. Dynamics to more than 1 m, allowing humans to walk on it, as we have already done with a group of 10 people. This floating Aquatic vegetation in the Pantanal changes over time, vegetation is most frequent in the Western zones, in the starting with free-floating plants such as Salvinia spp., Pistia sub-regions of Abobral and Cáceres and along the Paraguay, stratiotes, and Limnobium laevigatum (Humb. & Bonpl. Cuiabá, Negro, Miranda and Nabileque Rivers. The cover ex Willd.) Heine, which become colonised by the epiphyte of bursedge, O. cubense, mats can be distinguished on Oxycaryum cubense (Pott and Pott, 2003) and later by Landsat and SPOT images (Abdon et al., 1998). Eleocharis plicarhachis (Pivari et al., 2008). In more Swamps (“brejos”) or permanently flooded or waterlogged permanent ponds and oxbow lakes, aquatic vegetation tends areas are not as common as the rather misleading toponym to advance to a later stage of floating meadow, building Pantanal (= swampland) may suggest, and are confined up a floating organic soil (histosol) (Neiff, 1978, 1982), to wetter places and those with fine sediments, near which supports shrubs such as Ludwigia nervosa (Poir.) rivers, such as the Negro (sub-region Aquidauana), which Hara and Rhynchanthera novemnervia DC. (Pivari et al., overflows and disappears into a wide swamp, and parts of 2008) and even treelets, e.g. Cecropia pachystachya the sub‑regions of Abobral, Paraguay and Poconé. Also, Trécul and Tabebuia insignis (Miq.) Sandw., until the pond lately the increasingly flooded Taquari delta has become eventually dries up and the floating meadow dies, and the a swamp, due to silting of the river bed and consequent process resumes in a new flood cycle (Pott and Pott, 2003). permanent overflow (Pott and Pott, 2005). It contains Nitrophilous terrestrial plants also appear, such as Erechtites grasses and sedges, often with some becoming dominant hieracifolia (L.) Raf. ex DC., and the weedy tanner-grass such as giant sedge giganteus Vahl (“pirizal”), Urochloa arrecta (Hack. ex T. Durand & Schinz) Morrone Ipomoea carnea var. fistulosa (Mart. ex Choisy) D.F. Austin & Zuloaga thrives on this organic substratum. Often the (“algodoal”), fireflag Thalia geniculata L. (”caetezal”) floating meadow is not attached, as an island, and moves

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 255-263 257 Pott, VJ. et al. around by wind, sometimes becoming stranded on the shore (Figure 1); this is recommended for presence/absence data and decaying, recovering only if the water rises in time; it (Krebs, 1989). In addition, cluster analysis was performed can be carried downstream and block a channel mouth or using the Unweighed Pair Group Method with Arithmetic end up in the river, losing pieces due to collisions (banks, Mean (UPGMA) (Kent and Coker, 1992). logs) or storms (1 m waves), and finally disintegrating. 3.1. Types of aquatic habitats 2.6. Indicator species The types of aquatic habitats and vegetation sampled In the Pantanal, dominance of free-floating plants (Pistia, were river, “corixo” (anabranch, oxbow), floating meadow, Salvinia) indicates that the water body has dried off or the lake, pond, seasonal channel (“vazante”), backswamp and aquatic vegetation was removed by another disturbance. incoming stream. In the highlands, dense populations of Echinodorus The Alegre and Caracará Rivers are anabranches which macrophyllus (Kunth) Micheli, and Urospatha sagittifolia run in a cutoff channel from the Cuiabá River to lake Baía (Rudge) Schott indicate disturbed wetland, usually occurring dos Burros and other similar large open waters. The lakes near roads and on silted veredas (Pott and Pott, 2003), while show little aquatic vegetation cover, due to waves. Xanthosoma striatipes tends to increase under grazing. 3.2. Flora The submerged Ottelia brasiliensis Planch. increases in dammed streams. The floristic survey of various habitats at 17 sampling sites in the Park showed 135 species of aquatic macrophytes, 3. Pantanal Matogrossense National Park nearly half the total number for the whole Pantanal. The most numerous families were Poaceae (15), Cyperaceae As a case study, some original data extracted from the (10), Fabaceae (13), Onagraceae (9), (5), unpublished report are presented about the National Park, Convolvulaceae (5) and (5), and the best gathered by the authors in the year 2001. So far, there is represented genera were Ludwigia (13), Cyperus (10), no published work on the aquatic vegetation of this Park Ipomoea (6), Panicum (6), Aeschynomene (5), Eleocharis and the adjacent Acurizal Preserve. (5), Utricularia (5) and Polygonum (5). These families Seventeen sampling sites considered representative of and genera are typical of the Pantanal aquatic flora (Pott the aquatic habitats (Table 1) were established, inspected and Pott, 2000). by boat, or some on foot in the dry period, and plants were recorded at high and low waters. Plant specimens were 3.3. Life forms collected, and are kept at the CGMS (UFMS) Herbarium. The life forms are all present, albeit submerged, and Plots were not measured and varied in area. some rooted floating plants are not common in the Park. To obtain the floristic similarity among sampling sites It is surprising that not a single species of Nymphaea was of aquatic vegetation the Jaccard coefficient was used detected, even though it is so easy to spot, and that seven

Table 1. Types of aquatic habitats and vegetation sampled in Pantanal Matogrossense National Park and Acurizal Preserve, Pantanal wetland, Brazil. Sites Abbreviation Coordinates S, W Habitat Acurizal Preserve AP-1 17° 48’ 31.3” and 57° 34’ 34.8” Seasonal stream Acurizal Preserve AP-2 17° 48.47.5”and 57° 33’ 36.9” Oxbow lake (shallow) Baía Acurizal BA-1 17° 49’ 51.8”and 57° 34’ 55.4” Connected large oxbow Baía Caracará BC-1 17° 51.32” and 57° 26.86” Delta lake Baía Caracará BC-2 17° 51.71” and 57° 26.23” Delta lake Baía dos Burros BB-1 17° 50’ 23.7” and 57° 23’ 48.7” Closed oxbow Baía dos Burros BB-2 17° 49’ 19.6” and 57° 22.57.5” Oxbow lake Córrego Retiro CR-1 17° 50’ 29.8” and 57° 33’ 35.4 Incoming stream Córrego Zé Dias CZ-1 17° 52.06” and 57° 30.09” Bay of stream River Cuiabá RI-1 17° 51’ 08.3” and 57° 24’ 51.5” Backswamp Park houses PH-1 17° 50’ 45.4” and 57° 24’ 12.3” Pond Park houses PH-2 17° 50’ 44.7” and 57° 24’ 12.4” Backswamp River Alegre AL-1 17° 37’ 46” and 57° 24’ 46” Anabranch River Araminho AR-1 17° 44.05” and 57° 32.48” Old river bed River Araminho AR-2 17° 43.65” and 57° 32.37” Backswamp River Caracará RC-1 17° 43.22” and 57° 20.59” Anabranch River Caracará RC-2 17° 43.97” and 57° 19.81” Anabranch

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Figure 1. Dendrogram of fl oristic similarity among sampling sites of aquatic vegetation, grouped (separate vertical line on the right) according to their main habits, of Pantanal Matogrossense National Park and Acurizal Preserve, Pantanal wetland, Brazil. See Table 1 for names of sampling sites, coordinates and types of habitat. species are found elsewhere in the Pantanal. Their absence are an intermediate stage between the aquatic vegetation is attributed to the low transparency of the water not and early successional phases of riparian forest, held back allowing the young leaves to rise to the surface, although by fl ood and eventual wildfi res. Well developed fl oating their relative Victoria succeeds in this. The turbid water meadows occur on both sides of the anabranch Alegre would also explain the low number (fi ve) of submerged River (AL-1), with treelets of Tabebuia insignis (Miq.) species, four of them exclusive to the clear stream (CR-1) Sandw.), invaded by tanner-grass U. arrecta, while large coming from the hill. emergent plants dominate in the anabranch Caracará River (RC-2) until further upstream becoming blocked by fl oating 3.4. Main aquatic communities meadows. A typical oxbow lake (BB-1) is one connected Along rivers and streams there is a clear zoning of to the Baía dos Burros lake, with free-fl oating plants and vegetation, seasonally dynamic: rooted fl oating mat dead matter being colonised by the epiphytic Oxycaryum (Eichhornia azurea, Paspalum repens Berg., Panicum cubense plus dense mats of this sedge. Araminho River elephantipes Nees) near the bank, then a sequence of (AR) is an active old river bed, connected to the Paraguay emergent plants along the riverside, such as Panicum River and anastomosed with its own oxbows. dichotomifl orum Michx. and Paspalum fasciculatum Willd. on the levee, oxbows and backswamps with free 3.5. Species richness fl oating and emergent macrophytes, fl oating mats and Species richness (Table 2) increases in wave-protected fl oating meadows, and swamp of Aspilia latissima Malme. smaller water bodies and the older fl oating islands hold Thickets of this 1-2 m shrub, often mixed with Polygonum the highest number of species. On the fl oating meadow acuminatum Kunth, Ipomoea carnea Jacq. var. fi stulosa of the backswamp near the Park houses (PH-2) 45 species (Mart. ex Choisy) D.A. Austin, and Cissus spinosa Cambess. were found, nearly as many as on a fl oating meadow of

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Table 2. Species richness, exclusive and common species due to the advanced succession stage of AL-1 compared at sampling sites of aquatic vegetation of the Pantanal to RC-2, though both are on anabranches. Matogrossense National Park and Acurizal Preserve, Pantanal wetland, Brazil (meaning of site names with 3.7. Frequency and cover coordinates is given in Table 1). Common: present in Cover was visually estimated (in 1 m2 quadrats) for ≥ 7 habitats. the main species per sampling site. The most frequent Species species and also showing the highest cover is Polygonum Sites Richness Exclusive Common acuminatum, followed by Eichhornia crassipes with the PH-2 45 3 14 second highest frequency, while E. azurea is the second in AL-1 42 10 12 cover; the fourth in cover is Oxycaryum cubense (Table 3). So, only four species add to nearly half (46.7%) of the BC-2 40 0 15 overall cover of the sampled aquatic vegetation. Next in BC-1 34 1 13 frequency are Vigna lasiocarpa, Hymenachne amplexicaulis, AR-2 34 9 7 Mimosa pigra, Oxycaryum cubense, Aspilia latissima, CZ-1 27 4 11 Salvinia auriculata and Paspalum repens. BA-1 25 1 13 Even though Victoria amazonica is impressive in RI-1 23 1 9 the landscape, it is not frequent in the study area and its AR-1 22 1 8 population (Araminho River) was seen only during the flood period. This giant water-lily is very competitive BB-1 21 0 11 and tends to dominate other plants, expanding its 1-2 m PH-1 21 2 5 diameter leaves with their strong symmetric frame of RC-1 19 0 7 ironwork-like nerves, until a single individual can cover C-2 13 1 2 up to 20 m2. Associated species such as E. azurea and BB-2 13 0 5 Paspalum repens recolonise available space during the AP-1 12 2 5 low water season. AP-2 11 1 5 Near the inselberg Morro do Caracará the large populations of native rice Oryza latifolia Desv. and O. glumaepatula Steud. represent important germplasm, so the Park has a role in in situ conservation. At low water, the flood-grown culms lie down, and are then often taken the anabranch Alegre River (AL-1) with 42, each with one over by Hymenachne amplexicalis and Leersia hexandra, third of the aquatic floristic richness. The lowest richness until their regrowth from nodes when the flood returns. was found in two sites (AP-1 and 2) on floating mats of Lake Gaíva does not present macrophytes, only algae, the Paraguay River, at Acurizal Preserve, with 12 and indicated by the green colour of the water and the organic 11 species, respectively. sediment, and by filaments on the shore. 3.6. Floristic similarity 4. Use and Conservation Floristic similarity among sampled sites is shown in Figure 1. Cophenetic correlation explains 84% of the data. Domestic animals, particularly horses, feed on aquatic Two groups are shown in the dendrogram, A and B, with plants, mainly grasses and sedges (Pott and Pott, 2004; low similarity (15%). Group A joined sites AR-2, BB-2 Alho, 2008a,b). However, cows are usually removed from and PH-1, which are the Aspilia latissima backswamps, deep flooded areas or they spontaneously move to less with 25% similarity for the first two and 30% for the flooded ground. Nevertheless, cattle remain year-round third site. Two other sites stand out, CR-1 and RC-2, in rain-flooded zones, where they overgraze and trample with low similarity, below 10%; CR-1 is Córrego Retiro waterlogged short soft grasslands around ponds and drainage creek, with crystalline water from the hills, showing lines. Buffaloes are known for damaging aquatic habitats. submerged species (Utricularia breviscapa Wright ex For instance, Pott et al. (1999) found 18 aquatic plant Griseb., U. hydrocarpa Vahl, and Egeria najas Planch.) species in a pond with buffaloes, while 2 years after the and Ludwigia sedoides (Bonpl.) Hara, absent in the other removal of the animals the richness increased to 38 species. sampled sites, whereas RC-2 is an extensive bank of large Fortunately buffalo are not liked by traditional ranchers, emergent plants (A. latissima, I. carnea, Polygonum spp.). as they are difficult to manage and tend to become feral Group B was divided in two subgroups, b1 which linked in this extensive type of husbandry, otherwise aquatic AP-1 and AP-2, with 18% similarity, and b2 which joins vegetation could be severely damaged, as has occurred in sites AR-1, CZ-1, RC-1, RI-1, AL-1, BB-1, BA-1, PH-2, the Amapá wetlands in Amazonia. However, new owners BC-2, and BC-1, at different similarity levels (18 to 38%). have started to introduce buffalo again, as well as goats, Groupings tend to show a sequence from floating mats both of which present a threat to the Pantanal. (BB-1, BA-1, PH-2, BC-1 and 2) to inland sites farther from Wildfire reaching dry beds is deleterious to hydrophytes the Paraguay River. The floating meadows stayed apart with exposed buds, while it enhances seed germination of

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Table 3. Frequency and mean cover of the main aquatic macrophytes of Pantanal Matogrossense National Park and Acurizal Preserve, Pantanal wetland, Brazil. Species Frequency (%) Mean cover (%) Aspilia latissima Malme 58.82 3.53 Urochloa arrecta (Hack. ex T. Durand & Schinz) Morrone & Zuloaga 29.41 3.53 Cayaponia podantha Cogn. 29.41 1.12 Discolobium pulchellum Benth. 41.18 0.41 Echinochloa polystachya (Kunth) Hitchc. 29.41 0.18 Eichhornia azurea (Sw.) Kunth 58.82 11.24 Eichhornia crassipes (Mart.) Solms 64.71 12.24 Eleocharis minima Kunth 17.65 4.62 Hydrocotyle ranunculoides L.f. 29.41 - Hymenachne amplexicaulis (Rudge) Nees 47.06 0.65 Ipomoea carnea v. fistulosa (Mart. ex Choisy) Austin 35.29 3.70 Leersia hexandra Sw. 41.18 2.59 Lemna aequinoctialis Welw. 29.41 - Lippia alba (Mill.) N.E. Br. 35.29 0.76 Ludwigia helminthorrhiza (Mart.) Hara 41.18 - Ludwigia leptocarpa (Nutt.) Hara 29.41 1.12 Ludwigia nervosa (Poir.) Hara 35.29 - Melochia arenosa Benth. 41.18 2.47 Mimosa pigra L. 47.06 1.24 Oxycaryum cubense (Poepp.& Kunth)Lye 47.06 9.06 Panicum elephantipes Nees 41.18 2.24 Paspalum repens Berg. 47.06 3.59 Pfaffia glomerata (Spreng.) Pedersen 29.41 0.41 Pistia stratiotes L. 29.41 - Polygonum acuminatum Kunth 76.47 14.18 Polygonum ferrugineum Wedd. 35.29 3.88 Pontederia parviflora Alex. 41.18 - Rhabdadenia madida Miers 35.29 0.24 Salvinia auriculata Aubl. 47.06 1.94 Vigna lasiocarpa (Benth.) Verdc. 58.82 -

weedy Mimosa spp. and Sesbania virgata (Cav.) Pers., shrubs in the Pantanal National Park, where we observed that the which tolerate flooding and compete with other aquatic plants vigorous stoloniferous Panicum elephantipes is one of the (Pott and Pott, 2003). Yet rhizomatous macrophytes such only native grasses to match the competition. as Canna glauca L., Cyperus giganteus Vahl, Eleocharis Acknowledgements – To CNPq for the present research grant spp., Thalia geniculata and Typha domingensis can survive PQ2 to A. Pott and scholarship to LCP. Lima; to CAPES and tend to become dominant (op. cit.). for the scholarship to S.N. Moreira; to Prof. Dr. Geraldo A. Few exotic aquatic plants have invaded the Pantanal. Damasceno-Junior (UFMS) for statistical support; to José One is Sphenoclea zeylanica Gaertn. (Sphenocleaceae, Augusto Ferraz de Lima (director of Pantanal Matogrossense formely Campanulaceae), but it is restricted to the Paraguay National Park), Gislaine e Adalberto Eberhardt (Ecotrópica and Acurizal Preserve) and The Nature Conservancy for logistic River floodplain (Pott and Pott, 2000), even in undisturbed support; and to Dr. J.A. Ratter for critical review. sites such as the National Park. Two introduced grasses have become weeds, torpedo-grass Panicum repens L. References is spreading in sandy areas and tanner-grass Urochloa arrecta on clay (Pott and Pott, 2003). The latter is a real ABDON, MM., POTT, VJ. and SILVA, JSV., 1998. Avaliação threat to aquatic vegetation diversity, propagated by seed, da cobertura por plantas aquáticas em lagoas da sub-região da stolon, rhizome, or any fragment, carried by flood flow, Nhecolândia no Pantanal por meio de dados Landsat e SPOT. taking over other aquatic plants, as is already happening Pesquisa Agropecuária Brasileira, vol. 33, no. especial, p. 1675-1681.

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ALHO, CJR., 2008a. The value of biodiversity. Brazilian Journal POTT, A. and POTT, VJ., 1994. Plantas do Pantanal. Brasília: of Biology, vol. 68, no. 4, p. 1115-1118. Embrapa. 320 p. -, 2008b. Biodiversity of the Pantanal: response to seasonal -, 2004. Features and conservation of the Brazilian Pantanal. flooding regime and to environmental degradation. Brazilian Wetlands Ecology and Management, vol. 12, no. 6, p. 547-552. Journal of Biology, vol. 68, no. 4, p. 957-966. -, 2005. Alterações florísticas na Planície do Baixo Taquari. COSTA, LC. 2004. Florística de macrófitas aquáticas em duas In GALDINO, S., VIEIRA, LM. and PELLEGRIN, LA., Ed. lagoas e três vazantes do IPPAN na Fazenda Santa Emília, Impactos ambientais e socio-econômicos na Bacia do Rio Taquari, planície de inundação do Rio Negro, Pantanal, Mato Grosso Pantanal. Corumbá: Embrapa Pantanal. p. 261-293. do Sul. Campo Grande: Universidade para o Desenvolvimento do Estado e da região do Pantanal. Monografia de graduação do POTT, A., CUNHA, CN., POTT, VJ., SILVEIRA, EA. and curso de ciências biológicas. SARTORI, ALB., 2001. Relatório Final. Avaliação ecológica rápida: Componente botânica - Parque Nacional do Pantanal DA SILVA, CJ., 1984. Nota prévia sobre o significado biológico dos Matogrossense e entorno. In Plano de Manejo do Parque Nacional termos usados no Pantanal Mato-grossense, “batume” e “diquada”. do Pantanal Matogrossense. Ministério do Meio Ambiente. Anexo 4. Revista Universidade Federal de Mato Grosso, vol. 4, p. 30-36. POTT, VJ. and CERVI, AC., 1999. A família Lemnaceae Gray no GUGLIERI, A. and LONGHI-WAGNER, HM., 2004. Panicum Pantanal (Mato Grosso e Mato Grosso do Sul). Revista Brasileira (Gramineae - ) Flora Ilustrada do Rio Grande do Sul, de Botânica, v. 22, no. 2, p. 153-174. 26. Boletim do Instituto de Biociências UFRGS, vol. 59, p. 1-163. POTT, VJ. and POTT, A., 1997. Checklist das macrófitas HAMILTON, SK., ZIPPEL, SJ. and MELAK, JM., 1996. aquáticas do Pantanal, Brasil. Acta Botanica Brasilica, vol. 11, Inundation patterns in the Pantanal wetland of South America no. 2, p. 215-227. determined from passive microwave remote sensing. Archives of Hydrobiology, vol. 37, no. 1, p. 1-23. -, 2000. Plantas Aquáticas do Pantanal. Brasília: Embrapa. 404 p. HOEHNE, FC., 1923. Phytophysionomia do Estado de Matto -, 2003. Dinâmica da vegetação aquática do Pantanal. In THOMAZ, Grosso e ligeiras notas a respeito da composição e distribuição SM. and BINI, LM. Ecologia e manejo de macrófitas aquáticas. da sua flora. São Paulo: Cia. Melhoramentos. 94 p. Maringá: Editora da Universidade Estadual de Maringá. p. 145-162. -, 1948. Plantas aquáticas. São Paulo: Secretaria da Agricultura. POTT, VJ., 1998. A família Nymphaeaceae no Pantanal. Acta 168 p. Botanica Brasilica, vol. 12, no. 2, p. 183-194. IRGANG, BE., PEDRALLI, G. and WAECHTER, JI., 1984. -, 1999. Riqueza verde em meio azul. In SCREMIN-DIAS, E. Nos Macrófitos aquáticos da Estação Ecológica do Taim, Rio Grande jardins submersos da Bodoquena: guia para identificação das plantas do Sul, Brasil. Roessléria, vol. 6, p. 395-404. aquáticas de Bonito e região. Campo Grande: UFMS. p. 59-93. KENT, M. and COKER, P., 1992. Vegetation description and -, 2008. Plantas de ambientes aquáticos e úmidos do Centro-Oeste analysis: a practical approach. London: Belhaven Press. brasileiro. In Anais do 59o Congresso Nacional de Botânica. Natal: Sociedade Brasileira de Botânica. p. 441-442. KREBS, JC., 1989. Ecological methodology. New York: Harper Collins Publ. 654 p. POTT, VJ., BUENO, NC., PEREIRA, RAC., SALIS, SM. and VIEIRA, NL., 1989. Distribuição de macrófitas aquáticas numa LIMA, LCP., POTT, VJ. and SARTORI, ALB., 2006. Aeschynomene lagoa na Fazenda Nhumirim, Nhecolândia, Pantanal, MS. Acta L. (Leguminosae, Papilionoideae, Aeschynomeneae) no Estado de Botanica Brasilica, vol. 3, no. 2, p. 153-168. Mato Grosso do Sul, Brasil. Hoehnea, vol. 33, no. 4, p. 419-453. POTT, VJ., CERVI, AC., BUENO, NC. and POTT, A., 1999. MEIRELLES, ML., OLIVEIRA, RC., SANTOS, AR. and Dinâmica da vegetação aquática de uma lagoa permanente da CORREIA, JR., 2002. Espécies do estrato herbáceo e profundidade Fazenda Nhumirim, Pantanal da Nhecolândia, MS. In Anais do do lençol freático em áreas úmidas do Cerrado. Planaltina: II Simpósio sobre Recursos Naturais e Sócio-Econômicos do Embrapa Cerrados. 19 p. Boletim de Pesquisa e Desenvolvimento, Pantanal, Manejo e Conservação, 1996. Corumbá: Embrapa Embrapa Cerrados, no. 25. Pantanal. p. 227-235. NEIFF, JJ., 1978. Fluctuaciones de la vegetacion acuatica en PRADO, AL., HECKMAN, CW. and MARTINS, FR., 1994. ambientes en el valle de inundacion del Parana médio. Physics The seasonal succession of biotic communities in wetlands of the Sección B, vol. 38, no. 95, p. 41-53. tropical wet-and-dry climatic zone: II. The aquatic macrophyte vegetation in the Pantanal of Mato Grosso, Brazil. Internationale -, 1982. Esquema sucesional de la vegetacion en islas flotantes del Revue der gesamten Hydrobiologie und Hydrographie, vol. 79, Chaco argentino. Boletin de la Sociedad de Botánica, no. 4, p. 569-589. vol. 24, no. 1-4, p. 325-341. RAMOS, MVV., CURI, N., MOTTA, PEF., VITORINO, ACT., NUNES DA CUNHA, C., VILHALVA, DAA. and FERREIRA, FERREIRA, MM. and SILVA, MLN., 2006. Veredas do triângulo H., 2000. Espécies de campo inundável e de brejo, Fazenda Retiro Mineiro: solos, água e uso. Ciência Agrotécnica, vol. 30, no. 2, Novo, Pantanal de Poconé, MT (lista preliminar). In Anais do p. 283-293. III Simpósio sobre Recursos Naturais e Sócio-Econômicos do Pantanal - Os desafios do novo Milênio. Corumbá: Embrapa SAMPAIO, AJ., 1916. A flora de Matto Grosso: memória em Pantanal. p. 1-14. homenagem aos trabalhos da Comissão Rondon. Archivos do Museu Nacional, vol. 19, p. 1-125. PIVARI, MOD., POTT, VJ. and POTT, A., 2008. Macrófitas aquáticas de ilhas flutuantes (baceiros) nas sub-regiões do SCHESSL, M., 1999. Floristic composition and structure of Abobral e Miranda, Pantanal, MS, Brasil. Acta Botanica Brasilica, floodplain vegetation in the Northern Pantanal of Mato Grosso, vol. 22, no. 2, p. 563-571. Brazil. Phyton, vol. 39, no. 2, p. 303-336.

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SILVA, JSV., ABDON, MM. and POTT, A., 2007. Cobertura de levantamento aéreo. Revista Brasileira de Botânica, vol. 32, vegetal do bioma Pantanal em 2002. In Anais do XXIII Congresso no. 2, p. 143-152. Brasileiro de Cartografia. Rio de Janeiro: Sociedade Brasileira TAYLOR, PG., 1989. The Utricularia: a taxonomic de Cartografia. p. 1030 -1038. monograph. Kew: HMSO. 724 p. Royal Botanic Gardens. Kew Bulletin Additional Series, 14. SILVA, MP., MAURO, RA, MOURÃO, GM. and COUTINHO, TUR, NM., 1972. Um caso de epifitismo acuático. Boletin de M., 2000. Distribuição de classes de vegetação do Pantanal através la Sociedad Argentina de Botânica, vol. 10, no. 4, p. 323-327.

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Plant diversity of the Pantanal wetland Pott, A.a*, Oliveira, AKM.b, Damasceno-Junior, GA.a and Silva, JSV.c aDepartamento de Biologia, Universidade Federal de Mato Grosso do Sul – UFMS, CP 549, CEP 79070-900, Campo Grande, MS, Brazil bPrograma de Pós-graduação em Meio Ambiente e Desenvolvimento Regional, Universidade Anhanguera – Uniderp, Rua Alexandre Herculano, 1400, Jardim Veraneio, CEP 79037-280, Campo Grande, MS, Brazil cEmbrapa Informática na Agropecuária, CP 641, CEP 13083-886, Campinas, SP, Brazil *e-mail: [email protected] Received October 14, 2010 – Accepted December 13, 2010 – Distributed April 30, 2011

Abstract This is a review of current studies in diversity of the flora and main vegetation types in the Brazilian Pantanal. The flora of this wetland, nearly 2,000 species, constitutes a pool of elements of wide distribution and from more or less adjacent phytogeographic provinces, such as Cerrado, dry seasonal forests, Chaco, Amazonia and Atlantic Forest. The most numerous group includes wide-distribution species, mainly herbs, while the second contingent comes from the Cerrado. Endemic plants are rare, numbering only seven. The vegetation of the sedimentary floodplain is a mosaic of aquatics, floodable grasslands, riparian forests, savannas (cerrados), cerrado woodlands, dry forests, and a large area of mono-dominant savannas, and pioneer woodlands. The main vegetation types are briefly described with their characteristic species, and their estimated areas are given according to the latest mapping. Keywords: Cerrado, Chaco, flora, forest, savanna.

Diversidade de plantas do Pantanal

Resumo Esta é uma revisão sobre o estado do conhecimento sobre a flora e os principais tipos de vegetação do Pantanal brasileiro. A flora da planície inundável, de aproximadamente 2.000 espécies, é um encontro de elementos de ampla distribuição e de províncias fitogeográficas mais ou menos vizinhas, tais como o Cerrado, florestas estacionais, Chaco, Amazônia e Mata Atlântica. O grupo mais numeroso é de espécies de ampla distribuição, enquanto o segundo contingente vem do Cerrado. Plantas endêmicas são raras, somente sete. A vegetação da planície sedimentar é um mosaico de aquáticas, campos inundáveis, florestas ripárias, savanas (cerrados), cerradão, floresta decidual, e uma grande parte de savanas e florestas pioneiras monodominantes. Os principais tipos de vegetação são brevemente descritos em termos de espécies características, e suas áreas estimadas são dadas conforme o recente mapeamento. Palavras-chave: Cerrado, Chaco, flora, floresta, savana.

1. Introduction The history of the botany of the Pantanal goes back (Furtado et al., 1982; Loureiro et al., 1982; Abdon et al., to early European naturalists who visited the region, as 1998). The Brazilian botanist who most collected in Mato reported by Sampaio (1916). Later on, Hoehne (1923), Grosso and Mato Grosso do Sul was Hatschbach (Museu collecting beyond the confined areas along river routes, gave Botânico Municipal, Cutitiba), as can be verified in Dubs the first broader report on the vegetation and plant species (1988). Quite recently local botanists and collaborators of the old State of Mato Grosso, including the Pantanal. A have started to collect and to publish information on few geographers gave some landscape descriptions, with the flora (e.g., Pott and Pott, 1994, 1999, 2000) and the scanty reports of the vegetation. Veloso (1947, 1972) vegetation (e.g., Ratter et al., 1988; Nunes da Cunha and and Prance and Schaller (1982) gave some details on Junk, 2001; Damasceno-Junior et al., 2005; Nunes da vegetation types. With aerial photographs and the onset Cunha et al., 2007). of satellite imaging, a general view of the physiography A brief review will be given on the state of art concerning was shown and the first vegetation maps were produced diversity of vegetation types and main plants in the Pantanal.

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2. Results and Discussion covered with grasslands and floodable vegetation, with some woody elements of Cerrado. 2.1. Flora The other floristic province which influences the Considering only the Pantanal plain, 1,863 species region is the Amazon forest, mainly on the Paraguay River of phanerogams were listed, legumes being the most floodplains. The headwaters of many affluents of this river numerous (240 spp.), followed by more than 200 grasses begin near the transition with the Amazon basin and so (Pott and Pott, 1999). The list could be updated to nearly work as corridors for some species to reach the Pantanal, 2,000 species (Pott and Pott, 2009). The most numerous especially those from floodable areas (Igapó or Várzea) such families are Fabaceae (240), Poaceae (212), Malvaceae as Nectandra amazonum Nees, Victoria amazonica (Poepp.) (98), Cyperaceae (92), Asteraceae (87), Rubiaceae (62), J.C. Sowerby and Alchornea castaneifolia (Willd.) A. Juss., Myrtaceae (45), Convolvulaceae (41), and the best represented or occur in a similar wetland, the Araguaia floodplains, genera are Paspalum (35), Cyperus (29), Ipomoea (24), and Lhanos de Mochos, e.g. Vochysia divergens Pohl. The Panicum (22), Eugenia (20), Ludwigia (19), Mimosa flooding regime of the Paraguay River has a few months (18) and Rhynchospora (18) (Pott and Pott, 1999), with a lag after the rains fall on the upper watersheds, to reach prominence of herbaceous species, around 1,000, due to the Pantanal. So, when inundation occurs the dry season their adaptation to floodable areas, largely occupied by has already begun in the lowland, and even without local amphibious and grassland habitats. Pott and Pott (2000) rain the Amazon species can survive due to the floods. show 242 aquatic macrophytes, lately re-counted as 280 The next phytogeographical influence is the Chaco, species. There are 10 species of palms (Pott and Pott, which occurs mainly in Paraguay, Bolivia and Argentina. 1994), and two additional species of Bactris have been According to Prado et al. (1992) the real Chaco areas found, as yet unidentified. inside the Pantanal can be found only in Porto Murtinho. 2.2. Phytogeography Nevertheless, some Chaco species can be found in other sub-regions, and the most widespread is the palm Copernicia The central position of the Pantanal in South America alba Morong, which forms mono-dominant types in has allowed the encounter among distinct phytogeographic extensive areas, mainly in the South Pantanal. provinces, which are Amazonia to the North, the Cerrados Other types of flora characterising the Pantanal are to the East, the Meridional Forests to the South, and the the seasonal deciduous and semideciduous forests (dry Bolivian and Paraguayan Chaco to the West, favouring forests). Both occur on ancient levees (locally called a great variety of vegetation types, one of the reasons for the plural term “pantanals” (Adámoli, 1982; Alho, “cordilheiras”), mainly in the São Lourenço and Taquari 2008a,b; Oliveira, 2008). Uetanabaro et al. (2007, p. 280) fans. These formations have in fact two distinct origins. stated that the region lies within the “central portion of The semi-deciduous forest has floristic elements present the large diagonal area of open vegetation forms of South in the Brazilian Atlantic Forest, according to the official America, which goes from the Caatinga in Northeast Brazilian classification (IBGE, 1992), such as Albizia Brazil to the Chaco in Argentina, where areas of contact hassleri (Chodat) Burkart. The deciduous forest contains occur among Pantanal, Chaco and Cerrado”, qualifying floristic elements of the Pleistocene arch (Prado and Gibbs, it “of great biogeographic importance”. The Meridional 1993), found in the Chiquitania (Bolivia) and in Central Forests may be considered as the Paraná basin Forest Brazil in connection with the Caatingas of NE Brazil, (Spichiger et al., 2007). contributing with species such as Amburana cearensis Due to the floristic mix, with gallery forests, palmlands, (Allemão) A.C. Sm., Phyllostylon rhamnoides (J. Poiss.) floodable grasslands, Tabebuia aurea savannas, cerrados, Taub., brasiliensis Spreng., Seguieria aculeata cerrado grasslands, and flood-free ridges (paleodykes) Jacq., etc. Damasceno-Junior et al. (2009) estimated about covered with cerrado woodlands and forests, the vegetation 1.5 % of the Pantanal was covered with deciduous forests. used to be called “Pantanal Complex”, a concept dropped by Dry forests are mainly found on the calcareous hills of Adámoli (1982), considering “mosaic” a more proper term. Corumbá and on residual plateaus of Urucum-Amolar and The flora receives influence from some main Bodoquena, which are part of the Paraguay Upper Basin. neighbouring phytogeographic domains (Adámoli, 1982). 2.3. Main vegetation types The main influence is the group of wide distribution, mostly herbaceous species; around 160 of them are weedy. The According to Silva et al. (2000), Cerrado occupies second contingent is the Cerrado (with uppercase C when about 36 % of the region. There are various degrees of referring to a biogeographic province), connected to the Cerrado cover: more than 70% in the sub-regions of sandy highlands where the woody savanna called cerrados Aquidauana, Barão de Melgaço and Paiaguás (central (lowercase c to designate the vegetation form) are the and Eastern part of Pantanal); between 40 and 50% in main vegetation type. A great part of the areas inside the the sub-regions of Cáceres, Nhecolândia and Miranda; Pantanal with Cerrado have soils deposited by the Taquari and 10% in the sub-region of Poconé), whereas Cerrado River. The Taquari alluvial fan covers 50,000 km2, about vegetation is absent in the sub-regions of Nabileque and 30% of the Pantanal, but only a small part of it is actually Paraguay – with dominance of Chaco and Amazonian occupied by cerradão type woodland, while most of it is vegetation, respectively.

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According to Prance and Schaller (1982), Pott and Pterogyne nitens Tul., Tabebuia impetiginosa, Pott (1994, 2000) and Silva et al. (2000), there are T. roseo-alba (Ridl.) Sandw., etc; various vegetation types in the region, and mosaics of 3) Savanna, regionally called cerrado and which is floodable grasslands, cerrado woodland (cerradão), already internationally accepted, is found in areas cerrado, semideciduous forest, riparian forest, swamps with vegetation presenting xeromorphic features and floating vegetation are particularly conspicuous, plus due to the dry season, usually on dystrophic other physiognomies. A synthesis of vegetation types is soils, except for the forested type. Cerrado and given in Table 1. cerrado woodland (“cerradão”) on poor sands The Savanna (Cerrado) predominates in 50% of in the central and Eastern parts of the Pantanal the Pantanal. Flood dynamics causes rapid changes in show a lack of palms except for the small vegetation cover and promotes great diversity in pioneer Allagoptera leucocalyx (Drude) Kuntze, many types, varying from herbaceous to woody formations. In Fabaceae [Acosmium dasycarpum (Vog.) Yakol., general there is a continuum from semi-deciduous forests Andira cuyabensis Benth., Bowdichia virgilioides to dry and forested savanna (cerradão). The species listed Kunth, Hymenaea stigonocarpa (Mart.) Hayne, for the vegetation types described below were recorded Vatairea macrocarpa (Benth.) Ducke], Myrtaceae during field work on inspected remnants and are based on [Eugenia spp., Gomidesia palustris (DC.) Kausel, herbarium collection and the authors’ experience. Myrcia spp.], and Vochysiaceae [Qualea spp., 1) Seasonal Deciduous Forest (Tropical Dry Forest), Salvertia convallariodora A. St.-Hil., Vochysia found on rich or calcareous soils, presenting a spp.], Kielmeyera rubriflora Cambess. There tree stratum average 20 m tall with deciduousness are few hardwoods on poorer soils, used for above 50%, with two very distinct seasons (one fencing, usually legumes, e.g., Dipteryx alata rainy and another dry); it can be subdivided into: Vog., Diptychandra aurantiaca (Mart.) Tul., 1.1) Lowland Seasonal Deciduous Forest, Plathymenia reticulata Benth.; also Lafoensia commonly called dry forest, or calcareous pacari A. St.-Hil. Other common Cerrado trees: forest, with more than 60% of trees dropping Aspidospermum tomentosum Mart., Byrsonima their leaves; species include Anadenanthera coccolobifolia Kunth and Caryocar brasiliense colubrina (Vell.) Brenan, Aspidosperma Cambess. pyrifolium Mart., Myracrodruon urundeuva During dry years some cerrado and other pioneering Allemão, Phyllostylon rhamnoides, Tabebuia species “invade” grasslands, even occurring in dried-out impetiginosa (Mart. ex DC.) Standl., etc; pond beds: in sandy areas, dioica A. St.-Hil., 1.2) Submontane Seasonal Deciduous Forest, Bowdichia virgilioides, Buchenavia tomentosa Eichler, amongst several species, Acacia paniculata Caryocar brasiliense, Curatella americana L., Hymenaea Willd., Albizia hassleri, Anadenanthera stigonocarpa, Luehea paniculata Mart., Simarouba colubrina, Aspidosperma pyrifolium, versicolor A. St.-Hil., etc.; on clay, other species increase, M. urundeuva, etc. can be cited, but some are e.g. Callisthene fasciculata (Spreng.) Mart. and Tabebuia rare on the plain, such as Chorisia pubiflora aurea (Manso) Benth. & Hook. f. ex S. Moore, etc. (A. St.-Hil.) Dawson, Sterculia striata 3.1) Forested Savanna, called “Cerradão”, is a A. St.-Hil. & Naudin, or were not found, denser woodland where tree canopies touch e.g., Acosmium cardenasii H.S. Irwin & Arroyo, each other and part of the species are semi- Coutarea hexandra (Jacq.) K. Schum.; deciduous, 8 to 15 m tall, occurring more in 2) Seasonal Semi-deciduous Forest, characterised by the East and centre of the plain, on sandy soils leaf loss in 20 to 50% of trees, average 20 m tall, (sub-regions of Cáceres, Barão do Melgaço, reaching up to 30 m. It is subdivided into: Nhecolância, Aquidauana and Miranda), on 2.1) Alluvial Seasonal Semi-deciduous Forest, also flood-free ground; some of the species are: called riparian forest, found lining rivers of Byrsonima crassifolia (L.) Kunth, Caryocar the basin and often periodically flooded, with brasiliense, Dimorphandra mollis Benth., denser formations found mainly along the Eriotheca gracilipes (K. Schum.) Robyns, Paraguay River, in the sub-regions of Paraguay Kielmeyera coriacea Mart., Qualea grandiflora and Poconé, and along the São Lourenço River Mart., Q. parviflora Mart., Xylopia aromatica in Barão do Melgaço, with trees such as: Albizia (Lam.) Mart., etc; inundata (Mart.) Barneby & J.W Grimes, 3.2) Woody Savanna, also called cerrado Cassia grandis L.f., Vitex cymosa Bertero, etc; grassland, cerrado or open cerrado, is a form 2.2) Lowland Seasonal Semi-deciduous Forest, of cerrado stricto sensu, well represented in occurring on flood-free ground (ridges or ancient the Pantanal, with shrubs and scattered trees levees), with species such as: Anadenanthera up to 10 m tall, with thick bark and tortuous colubrina, Astronium fraxinifolium Schott, trunks, on a predominant grassy/herbaceous Attalea phalerata Mart. ex Spreng., Copernicia stratum, occurring more in the Eastern and alba, Protium heptaphyllum (Aubl.) Marchand, central parts of the plain, on sandy soils

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Table 1. Quantification (km2) of the vegetation cover of the Pantanal, mapping based on Landsat images of the year 2002. Vegetation names according to the official Brazilian nomenclature (IBGE, 1992), common terms in parentheses. Phytoecological region, formation or subtype Area (km2) I – Semi-deciduous Seasonal Forest Alluvial forest (riparian forest, gallery forest) 6,131.0 Submontane forest (dry forest) 92.3 II – Deciduous Seasonal Forest Alluvial forest (riparian forest, gallery forest) 9.6 Lowland forest (“Mata”, dry forest, calcareous forest) 519.0 Submontane forest (“Mata”, dry forest, calcareous forest) 910.0 III - Savanna (Cerrado) Forested (Cerrado woodland, Cerradão) 8,984.0 Wooded (Cerrado grassland, Cerrado, open Cerrado), with and without gallery forest 25,205.9 Grassy-Woody (Grassland, open grassland, bushy grassland, Elyonurus grassland, and 8,880.7 flooded grassland), with and without gallery forest Forested + Wooded and Wooded + Forested 80.3 Wooded + Grassy-Woody and Grassy-Woody + Wooded 734.5 IV – Steppic Savanna (Chaco) Wooded 213.3 Park (“Carandazal”) 6,590.7 Grassy-Woody (“campo”) 4,526.1 Wooded + Forested 80.3 Wooded + Grassy-Woody 244.2 Grassy-Woody + Grassy-Woody 490.3 V – Pioneer Formations: Vegetation with Fluvial and/or Lacustrine Influence: Mauritia palmland 5,216.2 (“Buritizal”), Spiny scrub (“Espinheiral”), Vochysia divergens woodland (“Cambarazal”), Giant sedge (“Pirizal”), tussock grassland (“Macega”), Couepia uiti woods (“Pateiral”), Licania parvifolia woods (“Pimenteiral”), Fireflag (“Caetezal”), Swamp, floating meadow and bushy grassland VI – Areas of ecological tension or floristic contacts Ecotone Savanna/Deciduous Seasonal Forest (“Mata”) 315.9 Savanna/Semi-deciduous Seasonal Forest (“Mata”) 2,258.5 Deciduous Seasonal Forest/Pioneer Formations (“Mata”) 4,697.4 Savanna/Pioneer Formations (Cerrado, Bushy Grassland, “Cambarazal”) 16,429.5 Steppic Savanna/Deciduous Seasonal Forest (“Mata”) 803.9 Enclave Savanna/Deciduous Seasonal Forest (“Mata”) 904.9 Savanna/Deciduous Seasonal Forest (“Mata”) 53.3 Savanna/ Semi-deciduous Seasonal Forest (“Mata”) 298.5 VII – Vegetation refuges (remnant communities): Herbaceous submontane refuge (Grassland) 28.4 VIII – Anthropic areas Secondary vegetation (of Savanna, Forest, Forested and Park Steppic Savanna) 403.6 Agriculture 411.5 Sown pasture (in Seasonal Forest, Savanna and Steppic Savanna) 16,511.8 IX – Other Anthropic Areas: Urban Influence + Mining degraded areas 132.7 X – Others: Water bodies (rivers, streams, oxbows, channels, lakes, ponds, brackish ponds) 2,557.3 TOTAL 151,186.2 Source: Silva et al. (2007).

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(sub-regions of Cáceres, Barão do Melgaço, such as Aposorella chacoensis (Morong) Paiaguás, Nhecolância, Aquidauana and Spegazz., Camptosema paraguariense Chodat Miranda), on lower areas, tending to grassland & Hassl., Dolichopsis paraguariensis (Benth.) as the degree of inundation increases, or the Hassl., Prosopis rubriflora Hassl., etc. (Pott, opposite, to woodier when drier. The most 1994), and because such vertic soils do not common species found are: Annona dioica, exist under Cerrado. Buchenavia tomentosa, Curatella americana, 3.4) Grassy-woody Savanna, called Campo or Dimorphandra mollis, Luehea paniculata, flooded grassland, normally made up of grasses Qualea parviflora, Simarouba versicolor and and herbs. It can be divided into flooded and Stryphnodendron obovatum Benth., among dry grasslands, the proportions varying in others; function of local rainfall and/or river overflow, 3.3) Park Savanna (Park of Cerrado) occurs in representing 31.1% of the vegetation of the floodable areas, normally with dominance of region, being more associated with drainage a single tree or shrub species over a grassy factor than soil fertility. Higher predominance stratum: in some portions of the Pantanal (Abobral, 3.3.1) Byrsonima orbignyana scrub (“canjiqueiral”) – Paiaguás, Nhecolândia and Nabileque), with homogeneous shrubby formation, 1-5 m tall, dominance of grasses and sedges. Among dominated by B. orbignyana A. Juss., on sandy coarse grasses [Andropogon spp., Paspalum or silty soils, floodable (ca. 50 cm deep), in carinatum Humb. & Bonpl., P. lineare Trin. and the sub-regions of Paiaguás, Nhecolândia, Trachypogon spicatus (L. f.) O. Kuntze], there Aquidauana, Abobral and Cáceres; as a pioneer are other species such as wild-rice Oryza spp., woody element, it is considered a pasture weed, Mesosetum spp., Reimarochloa spp., Paratheria and in past decades it was the main controlled prostrata Griseb., plus Paspalum spp., Digitaria species. Byrsonima orbignyana savanna, on spp., Panicum spp. Some species are found floodable sandy areas, also sometimes occurs more on poor soils, such as Axonopus purpusii on ancient silted drainage channels amongst (Mez) Chase, while Paspalum almum Chase Tabebuia aurea savanna and spread over most is associated with fertile soils. Grasslands, of the plain; depending on cycle of flood or drought, can be 3.3.2) Curatella americana (“lixeiral”) – a sort of taken over by woody vegetation of cerrado, or park savanna dominated by this tree, which vice-versa. occurs in floodable areas; often it is associated 4) Steppic Savanna, commonly called Chaco and with slightly higher ground, while it is a rather linked to the floristic province of Chaco in shrubby (multi-stem) dwarfed shrub on ill- Argentina, Paraguay and Bolivia; the only true drained land or a ca. 15 m tall tree in flood-free Brazilian Chaco occurs at the SW end of Mato woodland (Pott and Pott, 2004, 2005); it is the Grosso do Sul and belongs to the Chaco Húmedo most frequent woody species in the Pantanal, (Prado et al., 1992). There is a predominance being very abundant on the dystrophic sands of of spiny vegetation with features of semi-arid the Eastern zone (Pott and Pott, 2004), and in vegetation (presence of xeromorphic species, the earth-mound savanna in the Northern part plus cacti), with physiognomy similar to the of the floodplain (Ponce and Nunes da Cunha, Brazilian Caatinga, although it also contains wet 1993); it is also considered a weed by ranchers, areas, mainly in the Eastern Chaco; it is present mainly during dry years (Pott and Pott, 2004); on salty clays in the sub-regions of Nabileque and 3.3.3) Tabebuia aurea (“paratudal”) – floodable Porto Murtinho, and can be subdivided into four savanna with a single tree species stratum, vegetation forms: mean density of 363 individuals/ha (Soares 4.1) Forested Steppic Savanna, commonly called and Oliveira, 2009), 5-12 m tall, generally Chaco, dry forest or Chaquenian forest, with dry growing on a type of earth-mound or forest appearance, deciduous, average 5-7 m termite-like hummocks; other woody species tall; some typical species are Aspidosperma (e.g. Astronium fraxinifolium) appear in drier quebracho-blanco Schltdl., Caesalpinia years, but are kept back by wildfires or return paraguariensis (D. Parodi) Burkart, Diplokeleba of floods; occurs mainly in the South of the floribunda N.E. Br., Parkinsonia praecox (Ruiz Pantanal between the rivers Nabileque and & Pav. ex Hook.) J. Hawkins, Piptadenia Miranda, associated with slightly alkaline viridiflora (Kunth) Benth., Prosopis rubriflora, waters and sediments (Pott, 1994); it used P. ruscifolia Griseb., Schinopsis balansae Engl., to be interpreted as cerrado (Furtado et al., Zizyphus oblongifolius S. Moore, etc.; lately 1982; Loureiro et al., 1982), but lately it has undergoing strong deforestation; been considered to be linked to the Chaco flora 4.2) Steppic Scrub Savanna, also called Chaco, is (Silva et al., 2007), due to the associated species, similar to the previous one, but with shorter and

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spaced trees, interspersed in a stratum of spiny 5.3) Floating mats (“camalote”) and floating treelets which normally do not surpass 4 m, islands (“baceiro”, “batume”) – both found in such as Acacia farnesiana Willd., A. paniculata, permanent water bodies such as ponds, lakes, Capparis retusa Griseb., C. speciosa Griseb., canals, oxbows and rivers; floating mats are C. tweediana Eichl., Celtis pubescens Kunth, attached banks of floating macrophytes, or Zizyphus spp., etc., and frequently a ground not anchored, which then float downriver cover of Selaginella sellowii Hieron.; or move by wind; the main species are the 4.3) Steppic Park Savanna (“Carandazal”, “Campina water hyacinths Eichhornia crassipes (Mart.) de Carandá”) – made up of a grassy sward and a Solms and E. azurea (Sw.) Kunth, both rooted woody stratum with predominance of the palm or free-floating, and other aquatic plants, Copernicia alba, 8-20 m tall, occurring mainly water lettuce Pistia stratiotes L. and water in the Southern Pantanal, in large areas of the fern Salvinia auriculata Aubl., free-floating; sub-regions Nabileque and Porto Murtinho, on floating meadows have denser vegetation, made black alkaline or saline clays, with sub-surface up of grasses and sedges, mainly Oxycaryum calcium carbonate concretions; it also occurs cubense (Poepp. & Kunth) Lye and Eleocharis on sandy soils, if fertile or high pH, as around plicarhachis (Griseb.) Svens., rooted on brackish ponds (Nhecolândia) or shell-derived histosol (decomposing organic material) hummocks (Abobral), in floodable areas, while (Pivari et al., 2008) accumulated on the densely on drier patches it becomes denser, as palm entangled roots, most frequent in the sub- woodland, with associated species such as regions of Abobral and Cáceres and along the Capparis speciosa, Cereus bicolor Rizzini & rivers Paraguay, Cuiabá, Negro, Miranda and Mattos, Diplokeleba floribunda, Machaerium Nabileque; hirtum (Vell.) Stellf., Mimosa spp., Prosopis 5.4) Swamp (“brejo”) – permanently flooded or ruscifolia, Tabebuia nodosa (Griseb.) Griseb., waterlogged areas, except in drier years, are etc; confined to a few places, such as the Negro 4.4) Steppic Woody-grassy Savanna, various types River (Aquidauana) and sub-regions of Abobral, of grassland, such as open grassland, bushy Paraguay and Poconé; contains shrubby species, grassland, flooded grassland or spiny grassland, climbers, grasses and sedges, often forming made up of a grassy sward with spiny dwarf dense thickets of spiny shrubs (Byttneria filipes plants; common species: Acacia farnesiana, Mart. ex K. Schum., Mimosa weddelliana Celtis spinosa Spreng., C. pubescens, Mimosa Benth., etc.) and vines (Cissus spinosa spp., Paspalum simplex Morong, etc; Cambess., Combretum spp., Ipomoea spp.). 5) Pioneer formations or monodominant vegetation Giant sedge Cyperus giganteus Vahl (“pirizal”) types – areas under fluvial and/or lacustrine and fireflag Thalia geniculata L. (“caetezal”) is influence (sedimentation habitats, periodically or a sort of swamp or temporary pond dominated permanently flooded), made up of unstable ground covered by vegetation in constant succession, by these herbaceous species, mainly in the sub- such as Vochysia divergens, spiny scrub, giant regions of Abobral, Nabileque and Poconé, and sedge stands, plus others described below. increasing in the flooded Taquari delta; cat-tail This type of vegetation, a result of abiotic (soil Typha domingensis Pers. (“taboal”) is a similar and/or hydrological) factors, allows the presence tall aquatic herb which occurs in permanent of various types of association, few plant species or temporary ponds and increases in disturbed dominating large areas, forming typical landscapes flooded areas; with their local names in brackets: 5.5) Vochysia divergens woodland (“cambarazal”) 5.1) Attalea phalerata (“acurizal”) – homogeneous – homogeneous formation of an Amazonian or mixed forest understory made up of this tree, 5-18 m tall, on clay or loamy soils, tolerates shady palm, occurring on flood-free ridges periodical flood well, but not permanently; found and grooves and on river banks, which are mainly in the sub-regions of Barão do Melgaço, periodically flooded by flowing water; it often Poconé and Paraguay, adding up to 3.2% of the indicates anthropic action, as it can colonise Pantanal vegetation, in fact much more nowadays; cleared or frequently burned areas; it is a pioneer which forms dense pure stands, 5.2) Attalea speciosa palmland (“babaçual”) – considered a natural grassland weed for shading homogeneous dense forest predominantly of out grasslands (Allem and Valls, 1987). Since this palm, 10-22 m tall, occurring in the extreme 1980, large areas have been invaded on floodplains North of Cáceres sub-region and central of the Cuiabá and Paraguay rivers, now also on the Nhecolândia (0.3% of the region); some dry lower Taquari flooded delta (Pott and Pott, 2005), forest trees grow inside, held back by periodical but it slowly dies back under permanent deep fires, such as Astronium fraxinifolium; flood;

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5.6) Elyonurus muticus grassland (“caronal”), on leprosum Mart., Cordia glabrata (Mart.) A. intermediate, and only occasionally flooded or DC., Dipteryx alata, Myracrodruon urundeuva, flood-free sandy ground, lately being replaced Pisonia zapallo Griseb., Pouteria gardneri (Mart. to cultivate Brachiaria humidicola Rendle or & Miq.) Baehni, Pterogyne nitens, Rhamnidium other exotic grasses; elaeocarpum Reiss., Spondias mombin L., 5.7) Bromelia balansae stands (“gravateiro”) – Sterculia apetala Karst., Tabebuia impetiginosa, community of a pineapple-like plant, generally Zanthoxylum caribaeum Lam., etc. (Damasceno- indicating flood limit; when in large amounts Junior et al., 2009). The Chaco influence becomes inside groves and woods, it may indicate stronger southwards, as in the areas of Soldado selective logging with opening of gaps, which and Porto Murtinho. Some of the dry forest areas allow fast growth and spread, blocking passage can be interpreted as a junction of many ancient of large animals, then the leaves have very levees, generally an alluvial fan built at the earlier spiny edges; it is not viable to map it yet; encounter of a tributary with the calm flood waters 5.8) Couepia uiti scrub (“pateiral”) – native of a larger river. For example, sediments of the grassland area invaded by this tree species, Taquari River were deposited where they met the considered a weed (pioneer), being abundant still flood waters of the Paraguay River, before the on sandy soils on floodplain and among riparian Paraguay was gradually pushed westwards. vegetation; • Riparian forests – Most information on gallery 5.9) Licania parvifolia scrub (“pimenteiral”) – native forests is given by Damasceno-Junior et al. (2005), grassland areas invaded by this pioneer tree, for the Southern part of the Pantanal, and by occurring over nearly the whole Pantanal Nunes da Cunha and Junk (2001), for the Northern floodplain; sub-regions. Some riparian trees are sort of 5.10) Tabebuia heptaphylla woods (“piuval”), generalists, found along almost every water course, a deciduous tree occurring in savanna or such as Andira inermis Kunth and Inga vera ssp. woodland, in floodable areas, generally not far affinis (DC.) T.D. Penn., whereas others tend to be from rivers and seasonal streams, tending to more frequent on heavily flooded clay, e.g., Albizia riparian forest in the succession; inundata and Sapium obovatum Klotzsch ex Müll. 5.11) Mauritia flexuosa palmland (“buritizal”) – Arg. In the Northern section of the Paraguay River almost homogeneous formation of “buriti” on the plain a few grow in nearly pure stands, such palm, 5-15 m tall, with restricted distribution as Erythrina fusca Lourt. and S. obovatum, often near the Eastern border of the plain, along the like orchards, and some Amazonian species occur Aquidauana and Taquari Rivers, and in Barão which have not been found much downstream, de Melgaço; such as Brosimum lactescens (S. Moore) Berg 5.12) Erythrina fusca woods (“abobral”) – one of and Sloanea garckeana K. Schum., plus an as yet the main trees, usually in groups, along the unidentified red-fruited species of Bactris. Along Paraguay River in the Cáceres sub-region, also some outgoing temporary streams (diffluents) of spread along the margins of the Aquidauana the Taquari River, there occur dense stands of river; the flowers are visited by psittacids; Tapirira guianensis Aubl., hardly seen elsewhere 5.13) Xylopia aromatica savanna (“pindaival”) – in the Pantanal. It seems rather paradoxical that Cerrado tall shrub or tree community common some trees share very distinct habitats, such as in the NE of the plain. the riverside and dry forests; for example, Albizia hassleri and Vitex cymosa. Many species of gallery 2.4. Remarks upon vegetation types forests of upland streams do not grow on the plain, • Dry forests – Dry forests, more abundant on the or only as far as the river is fast-flowing, such as hills rather than on the plain (Hoehne, 1923; Hirtella gracilipes (Hook. F.) Prance and Licania Prance and Schaller, 1982; Ratter et al., 1988), humilis Cham. & Schltdl. on the Taquari River, were recently described in more detail by still close to the Eastern border. A curious case Damasceno-Junior et al. (2009). This vegetation is Salix humboldtiana Willd., which has restricted type covers c. 4% of the Pantanal, as few occurrence on sandy levees of the Aquidauana significant areas occur on the plain: Mata do River at the very entrance to the plain; after a Cedro and Fuzil in Paiaguás, Mata do Bebe in disjunction it reappears on heavy clay along the Barão de Melgaço, and other scattered patches Paraguay River at the far end of the Pantanal. in South Poconé, Abobral, Miranda, around Below Corumbá the Paraguay River does not brackish ponds in SE Nhecolândia, Soldado often exhibit a proper riparian forest, but pioneer and Porto Murtinho (Damasceno-Junior et al., stages of flexible shrubs, which withstand flood 2009). Typical species are: Acrocomia aculeata flow, such as Alchornea castaneifolia. (Jacq.) Lodd. Ex Mart., Astronium fraxinifolium, Due to the dynamics of the rivers, strips of “old” forest Casearia gossypiosperma Briq., Combretum are eroded away and new ones start on the opposite bank,

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 265-273 271 Pott, A. et al. where sediments accumulate and become first colonised by Nees, Mesosetum cayennense Steud., Panicum stenodes aquatic plants, often nearly mono-dominant, mainly grasses Griseb.] (Pott, 1988). (Panicum dichotomiflorum Michx., P. pernambucense 2.5. Endemic and rare species (Spreng.) Mez ex Pilg., Paspalum fasciculatum Willd.) and sedges (Cyperus, Fuirena, Rhynchospora), Polygonum As the Pantanal is a geologically-recent (Holocene) spp., then subshrubs [Aspilia latissima Malme, Ipomoea Quaternary floodplain, very few endemic species have been carnea var. fistulosa (Mart. ex Choisy) D.F. Austin], shrubs found, such as Arachis diogoi Hoehne, A. hoehnei Krapov. (Alchornea castaneifolia), later trees, all entangled with a & W.C. Greg., or new and also endemic plant species, e.g. great mass of vines, such as Combretum lanceolatum Pohl, Arachis vallsii Krapov. & W.C. Greg., Euplocca pottii J.I.M. Cissus spinosa, Mikania spp. Some of the main species Melo, Habranthus pantanensis Ravenna, of riparian forests are: a) early stage of succession with pantanalensis H. Rob., Xanthosoma pottii E.G. Gonçalves. Cecropia pachystachya Trécul, Ruprechtia brachysepala Some are endemics in the broad sense, such as Bergeronia Meisn., Inga vera, Sapium obovatum and Vochysia divergens; sericea Mich. and Lonchocarpus nudiflorens Burkart. There b) late successional stage trees are, for example Erythrina seem to be more endemic plants on surrounding hills than fusca, Ficus spp., Genipa americana L., Pouteria glomerata on the plain, such as Aspilia grazielae Santos, Discocactus (Miq.) Radlk. and Triplaris americana L. Succession stages ferricola Buining & Bradero, Gomphrena centrota Holzh., frequently occur in progressive chronological zoning, but G. matogrossensis Suessenguth, Lonchocarpus variabilis R.R. are also intermingled due to gaps caused by flood or fire. Rodrigues & Tozzi, Mentzelia corumbaensis Hoehne, Mimosa Along seasonal streams often grows a hedgerow of Licania ferricola R.R. Silva & A.M.G.A. Tozzi, Deuterocohnia parvifolia Hub., sometimes Calophyllum brasiliense meziana Kuntze ex Mez, etc. Cambess. The sequence described here depends on the • Rare species: Cereus saddianus Rizz. & Mattos, level of inundation that the considered river can reach, Dieffenbachia aglaonematifolia Engl., and on the region drained. Discolobium psoralifolium Benth., Eichhornia Riparian species may grow many kilometres from the diversifolia (Vahl) Urb., Evolvulus pterygophyllus river, such as Combretum lanceolatum, Licania parvifolia Mart., Eulophia alta (L.) Fawc. & Rendl., and Vochysia divergens, often in closed mono-dominant Habenaria nabucoi Ruschi, Ipomoea piresii populations, therefore frequently considered undesirable O’Donell, Ludwigia affinis (DC.) Hara, Nymphaea invasive woody plants, as they may take over and even belophylla Trickett, Utricularia trichophylla shade out useful grasslands. Spruce ex Oliv., Xanthosoma aristiguietae • Grasslands – Allem and Valls (1987) produced the (Bunting) M. Madison. first comprehensive study, a benchmark on natural grasslands of the Pantanal. Grasslands are by far Acknowledgements – To Dr. J.A. Ratter for suggestions on the the biggest vegetation type of the Pantanal. Often manuscript. The author A. Pott is grateful to CNPq and CAPES for the present research grants PQ2 and PVNS, and JSV. Silva the open landscape is mistaken for deforested area, thanks for the fund of the PROBIO-Pantanal Project (Ministério instead of natural vegetation due to seasonal flood, do Meio Ambiente/Embrapa/SEMACT-MS). even though there is some spotty shrub control done by ranchers. The effect of flood holding back References woody vegetation can be observed during years without flood, when grasslands become shrubby, ABDON, MM., SILVA, JSV., POTT, VJ., POTT, A. and SILVA, as during the last 15 years. MP., 1998. Utilização de dados analógicos do Landsat‑TM na Grassland composition depends so much on flood level discriminação da vegetação de parte da sub-região da Nhecolândia that a few centimetres difference is enough to determine no Pantanal. Pesquisa Agropecuária Brasileira, vol. 33, no. especial, change in species. Besides the main grasses, there is a great p. 1799-1813. number of herbaceous plants, annuals or perennials, most ADÁMOLI, J., 1982. O pantanal e suas relações fitogeográficas of them growing in particular conditions of flood or soil, com os cerrados. Discussão sobre o conceito de “Complexo do and these may be indicators, for example: therophytes or Pantanal”. In Anais do XXXII Congresso Nacional de Botânica. annual species propagated by seed (Bacopa arenaria (J.A. Teresina. p. 109-119. Smith) Edwall, Heliotropium filiforme Lehm., Ludwigia ALHO, CJR., 2008a. The value of biodiversity. Brazilian Journal octovalvis (Jacq.) Raven, Sacciolepis myuros (Lam.) of Biology, vol. 68, no. 4, p. 1115-1118. Chase); indicators of clay [annuals Brachiaria adspersa (Trin.) Parodi, Eriochloa punctata (L.) Desv., Heliotropium -, 2008b. Biodiversity of the Pantanal: response to seasonal procumbens Mill., and perennials Hemarthria altissima flooding regime and to environmental degradation. Brazilian Journal of Biology, vol. 68, no. 4, p. 957-966. (Poir.) Stapf & Hubb., Paspalum millegrana Schrad.]; indicators of salinity [annuals Microchloa indica (L.f.) ALLEM, AC. and VALLS, JFM., 1987. Recursos forrageiros Beauv., Sporobolus pyramidatus (Lam.) Hitchc., Tripogon nativos do Pantanal Mato-grossense. Brasília: Embrapa. 339 p. spicatus (Nees) Ekm., and perennial Paspalum vaginatum DAMASCENO-JUNIOR, GA., POTT, A. and SILVA, JSV., Sw.]; and indicators of poor soils [Gymnopogon spicatus 2009. Florestas estacionais do Pantanal, considerações florísticas e (Spreng.) O.Kuntze, Leptocoryphium lanatum (H.B.K.) subsídios para conservação. Geografia, vol. 34, no. 143, p. 697-707.

272 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 265-273 Plant diversity of Pantanal

DAMASCENO-JUNIOR, GA., SEMIR, J., SANTOS, FAM. and -, 2005. Alterações florísticas na Planície do Baixo Taquari. LEITÃO-FILHO, HF., 2005. Structure, distribution of species In GALDINO, S., VIEIRA, LM. and PELLEGRIN, LA., Ed. and inundation in a riparian forest of Rio Paraguai, Pantanal, Impactos ambientais e socio-econômicos na Bacia do Rio Taquari, Brazil. Flora, vol. 200, no. 2, p. 119-135. Pantanal. Corumbá: Embrapa Pantanal, p. 261-293. DUBS, B., 1988. Prodromus Florae Matogrossensis. Betrona -, 2009. Vegetação do Pantanal: fitogeografia e dinâmica. In Verlag: Küssnacht. 444 p. Anais do II Simpósio de Geotecnologias no Pantanal. Corumbá: Embrapa Informática Agropec./INPE. p. 1065-1076. FURTADO, PP., GUIMARÃES, JG., FONZAR, BC. and PIRES, JM., 1982. Vegetação. In Ministério das Minas e Energia. Projeto POTT, VJ. and POTT, A., 2000. Plantas Aquáticas do Pantanal. Radambrasil. Folha SF.21 Campo Grande. Rio de Janeiro: Secretaria Brasília: Embrapa. 404 p. Geral. p. 281-333. Levantamento de Recursos Naturais, 28. PRADO, PE. and GIBBS, PE., 1993. Patterns of species distribution HOEHNE, FC., 1923. Phytophysionomia do Estado de Matto in the dry seasonal forests of South America. Annals of the Grosso e ligeiras notas a respeito da composição e distribuição Missouri Botanical Garden, vol. 80, p. 902-927. da sua flora. São Paulo: Cia. Melhoramentos. 94 p. PRADO, PE., GIBBS, PE., POTT, A. and POTT, VJ., 1992. The Instituto Brasileiro de Geografia e Estatística – IBGE, 1992. Chaco-Pantanal transition in southern Mato Grosso, Brazil. In Manual técnico da vegetação brasileira. Rio de Janeiro: IBGE. FURLEY, PA., PROCTOR, J. and RATTER, JA., Ed. Nature 92 p. Séries Manuais Técnicos em Geociências, no. 1. and Dynamics of Forest-Savanna Boundaries. London: Chapman & Hall. p. 451-470. LOUREIRO, RL., LIMA, JPS and FONZAR, BC., 1982. Vegetação. In Ministério das Minas e Energia. Projeto Radambrasil. Folha PRANCE, GT. and SCHALLER, G., 1982. Preliminary observations SE.21 Corumbá e parte da Folha SE.20. Rio de Janeiro: Secretaria on vegetation types of the Pantanal, Mato Grosso, Brazil. Brittonia, Geral. p. 329-372. Levantamento de Recursos Naturais, no. 27. vol. 34, no. 2, p. 228-251. NUNES DA CUNHA, C. and JUNK, WJ., 2001. Distribution of RATTER, JA., POTT, A., POTT, VJ., CUNHA, CN. and woody plant communities along the floodplain gradient in the HARIDASAN, M., 1988. Observations on woody vegetation Pantanal of Poconé, Mato Grosso, Brazil. International Journal types in the Pantanal and at Corumbá, Brazil. Notes from the of Ecology and Environmental Sciences, vol. 27, no. 2, p. 63-70. Royal Botanic Garden of Edinburgh, vol. 45, no. 3, p. 503-525. NUNES DA CUNHA, C., JUNK, WJ. and LEITÃO-FILHO, HF., SAMPAIO, AJ., 1916. A flora de Matto Grosso: memória em 2007. Woody vegetation in the Pantanal of Mato Grosso, Brazil: homenagem aos trabalhos da Comissão Rondon. Archivos do a preliminary typology. Amazoniana, vol. 19, no. 3/4, p. 159-184. Museu Nacional, vol. 19, p. 1-125. OLIVEIRA, AKM., 2008. Pantanal – origens e características SILVA, JSV., ABDON, MM. and POTT, A., 2007. Cobertura gerais. In OLIVEIRA, AKM., GARNÉS, SJA. and FAVERO, vegetal do Bioma Pantanal em 2002. In Anais do XXIII Congresso S., Ed. Meio ambiente e produção interdisciplinar: sociedade, Brasileiro de Cartografia. Rio de Janeiro: Sociedade Brasileira natureza e desenvolvimento. Campo Grande: Uniderp. p. 11-25. de Cartografia. p. 1030 -1038. PIVARI, MOD., POTT, VJ. and POTT, A., 2008. Macrófitas SILVA, MP., MAURO, R., MOURÃO, G. and COUTINHO, aquáticas de ilhas flutuantes (baceiros) nas sub-regiões do M., 2000. Distribuição e quantificação de classes de vegetação Abobral e Miranda, Pantanal, MS, Brasil. Acta Botanica Brasilica, do Pantanal através de levantamento aéreo. Revista Brasileira de vol. 22, no. 2, p. 563-571. Botânica, vol. 23, no. 2, p. 143-152. PONCE, VM. and NUNES DA CUNHA, C., 1993. Vegetated SOARES, JJ. and OLIVEIRA, AKM., 2009. O paratudal do earth mounds in tropical savannas of Central Brazil: a synthesis Pantanal de Miranda, Corumbá, MS, Brasil. Revista Árvore, with special reference to the Pantanal do Mato Grosso. Journal vol. 33, no. 2, p. 339-347. of Biogeography, vol. 20, p. 219-225. SPICHIGER, R., BISE, B., CALENGE, C. and CHATELAIN, POTT, A., 1988. Pastagens no Pantanal. Corumbá: EMBRAPA- C., 2007. Biogeography of the Forests of the Paraguay-Paraná CPAP. 58 p. Documentos, no. 7. Basin. In PENNINGTON, T., LEWIS, GP. and RATTER, JA., Ed. Neotropical savannas and seasonally dry forests, plant -, 1994. Ecossistema Pantanal. In: PUIGNAU, JP., Ed. Utilización diversity, biogeography and conservation. Boca Raton: Francis y manejo de pastizales. Montevideo: IICA-PROCISUR. p. 31-44. & Taylor. p. 193-211. IICA-PROCISUR Diálogo, no. 40. UETANABARO, M., SOUZA, FL., LANDGREF FILHO, P., POTT, A. and POTT, VJ., 1994. Plantas do Pantanal. Brasília: BEDA, AF. and BRANDÃO, RA., 2007 Anfíbios e répteis do Embrapa. 320 p. Parque Nacional da Serra da Bodoquena, Mato Grosso do Sul, Brasil. Biota Neotropica, vol. 7, no. 3, p. 279-289. -, 1999. Flora do Pantanal – listagem atual de fanerógamas. In Anais do Simpósio sobre Recursos Naturais e Sócio-Econômicos VELOSO, HP., 1947. Considerações sobre a vegetação de Mato do Pantanal, Manejo e Conservação, 2, 1996. Corumbá: Embrapa Grosso. II. Notas preliminares sobre o Pantanal e zonas de transição. Pantanal. p. 297-325. Memórias do Instituto Oswaldo Cruz, vol. 45, p. 253-272. -, 2004. Features and conservation of the Brazilian Pantanal. -, 1972. Aspectos fito-ecológicos da Bacia do Alto Paraguai. São Wetlands Ecology and Management, vol. 12, no. 6, p. 547-552. Paulo: USP. USP, Biogeografia, no. 7.

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The floristic heterogeneity of the Pantanal and the occurrence of species with different adaptive strategies to water stress Scremin-Dias, E.a*, Lorenz-Lemke, AP.a and Oliveira, AKM.b aDepartamento de Biologia, Centro de Ciências Biológicas e da Saúde, Universidade Federal de Mato Grosso do Sul – UFMS, Cidade Universitária, s/n, CP 549, CEP 79070-900, Campo Grande, MS, Brazil bPrograma de Pós-graduação em Meio Ambiente e Desenvolvimento Regional, Universidade Anhanguera-Uniderp, Rua Alexandre Herculano, 1400, Jardim Veraneio, CEP 79037-280, Campo Grande, MS, Brazil *e-mail: [email protected] Received October 14, 2010 – Accepted December 13, 2010 – Distributed April 30, 2011

Abstract The Pantanal is characterised by a diversity of environments with areas ranging from periodic or permanent heavy flooding to areas with low flood levels, and even environments that never flood. Plant species which inhabit the floodplain are distributed in specific niches, with influence of various phytogeographic domains, including the Seasonal Semi‑deciduous Forest, Amazon Rainforest, Cerrado and Chaco, as well rocky remnants, with a wide ecological span in their components. In intensely flooded areas, aquatic macrophytes are widely distributed, with their dynamics closely linked to time, depth and extent of flooding. Although the term “Pantanal” suggests a huge swamp-type wetland, water level variation during a seasonal cycle does not directly reach the root system of many plants. The landscape diversity of the Pantanal wetland is molded by the flood pulse, which interferes with the dynamics of plant communities. Therefore, the retraction and expansion of populations or communities is reflected in important ecological characteristics, considering the variety of morphological, anatomical and ecophysiological features of the species, whose phenotype is the result of a particular genotype. The present study discusses peculiar issues in the adaptation of species distributed in the Pantanal biome and underscores the importance of multidisciplinary approaches to obtain conclusive data on adaptive studies. Keywords: flood pulse, ecophysiological features, adaptation of species.

A heterogeneidade florística do Pantanal e a ocorrência de espécies com diferentes estratégias adaptativas ao estresse hídrico

Resumo O Pantanal caracteriza-se pela diversidade de ambientes com áreas que variam desde intenso alagamento, periódico ou permanente, a áreas com baixo índice de alagamento até ambientes nunca alagados. Espécies vegetais que habitam a planície distribuem-se em nichos específicos, com influência de vários domínios fitogeográficos, entre eles a Floresta Estacional Semidecidual, Floresta Amazônica, Chaco e Cerrado, além de remanescentes rochosos, prevalecendo grande amplitude ecológica de seus componentes. Nas áreas de intenso alagamento, macrófitas aquáticas se distribuem amplamente, com dinâmica intimamente ligada ao tempo, intensidade e amplitude de alagamento. Apesar de o termo Pantanal induzir a ideia de ambiente de alagamento intenso, para muitas espécies, as variações do nível da água num ciclo sazonal não atingem o sistema radical diretamente. A diversidade de paisagens na planície é moldada pelo pulso de inundação que interfere diretamente na dinâmica das comunidades de plantas. Assim, retração ou expansão de populações ou comunidades, reflete características ecológicas importantes, a exemplo do aparato morfológico, anatômico e ecofisiológico das espécies, cujo fenótipo é resultante de genótipo particular. Neste trabalho, são discutidas questões peculiares sobre a adaptação das espécies distribuídas no bioma Pantanal e ressaltada a importância de abordagens multidisciplinares para obtenção de dados conclusivos em estudos adaptativos. Palavras-chave: pulso de inundação, aparatos ecofisiológicos, adaptação de espécies.

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 275-282 275 Scremin-Dias, E., Lorenz-Lemke, AP. and Oliveira, AKM.

1. Diversity of Environments of the Pantanal phytophysiognomies of these provinces are mixed in the Wetlands Pantanal wetlands, in floodable and flood-free areas, in edge areas and on the plateaus. The Pantanal is characterised by the heterogeneity Alho (2008a,b) emphasises the remarkable combination of vegetation units, which occupy distinct environments of xerophytic and mesophytic vegetation growing side by created by fluvial morphogenesis (Adámoli and Pott, 1996; side in seasonally flooded areas in the Pantanal. Tree and Oliveira, 2007). Several plant families inhabit typical shrub species occur at periodically flooded spots, or in floodable fields, widely distributed in the Pantanal wetland areas not subjected to the flood pulse effect of the annual depressions, as well as the cordilheiras (strands of elevated cycle. However, many herbaceous plants and aquatic soil with unflooded woody vegetation) and capão (circular macrophytes occur in areas with particular water variation or elliptical forest distributed on periodically flooded or those permanently flooded. Thus, the Pantanal landscape natural grassland matrix) (Damasceno-Junior et al., 1999). is shaped by water regime, and its dynamics reflect the local In the Pantanal wetlands, which constitute about 35% of rainfall and, mainly, changes in water level corresponding the Upper Paraguay River Basin (Bacia do Alto Paraguai) to rainfall in the headwaters of Paraguay River tributaries. area, several minor watersheds drain large headwater The floristic composition of a certain region is dynamic areas, which are responsible for the vast flood area of and probably continues to change over time. On a local the plain. Although the Pantanal is associated with the scale, this can be exemplified by the seasonal cycle of Paraguay River floodplain and its tributaries, along the the Pantanal, where, due to its multiannual period of wetland occur microbasins arising from the residual relief flood and drought with distinct intensity and duration hills throughout the entire western edge of the Pantanal (Pott and Adámoli, 1996), the species succession and (Abdon and Silva, 2006). composition in flooded fields is peculiar, and therefore Among the landscape units the Urucum Residual Plateau the population dynamics is markedly affected by water (Planalto Residual do Urucum) stands out, a formation regime. The retraction or expansion of the populations which holds the Maciço do Urucum, a priority area for or communities are reflected by important ecological conservation, because of its composition and richness of characteristics, considering the variety of morphological, plant species (Brasil, 1999) and endemism. It presents anatomical and ecophysiological features of the species, isolated hills located in low areas, with altitudes between whose phenotypes are the result of a particular genotype 300 and 1000 m, entisols and podzol and low humic (Fahn and Cutler, 1992). gley, covered by submontane seasonal semi-deciduous When analysing the morphoanatomical adaptations of forest and lowland forests (Alho and Gonçalves, 2005). Pantanal plants, it is possible to classify them according to Damasceno‑Junior et al. (2005) cite the rocky vegetation their habitats: species that inhabit regions strongly influenced formations, shrubby grassland (campo sujo), cerrado, closed by flood pulse – Pantanal sensu stricto –, and those regions woodland (cerradão) and semi-deciduous and deciduous which are not influenced by periodic flood – Pantanal forests, as the phytophysiognomies of this formation. sensu lato (which comprise all species distributed in the The remnants of rock formations of limestone, sandstone, biome). Plant species or communities that naturally grow in iron and manganese distributed singly or in North-South axis a given environment share morphoanatomical characteristics ridges in the wetland, currently suffer major anthropogenic and compatible physiological balances (Larcher, 2004; pressure to extract ore. These areas hold grasslands with Fahn and Cutler, 1992), which make them adapted to that particular flora along an altitudinal gradient and, although particular condition. For Fahn and Cutler (1992), adaptation the floristic inventories are still insufficient to determine the results from the interrelationships of living organisms and species richness, there is apparently a considerable degree the environment they inhabit and from the evolutionary of endemism, with the occurrence of Aspilia grazielae, changes throughout the life history of several classes of Gomphrena centrota (Pott et al., 2000) and Vernonia pottii organisms in their particular environment. (Esteves, 2005) being reported on these rock formations. Thus, understanding the structure of plant organs and In the low altitude areas the endemic species Arachis tissues in relation to the environment for which they were diogoi, A. vallsii, Maranta pantanensis, Stilpnopappus selected during their evolutionary course, involves studies pantanalensis and Xanthosoma pottii stand out (Pott and of ecological anatomy, and these must be conducted in Pott, 2009). It is suggested that the low level of endemism a multidisciplinary way, complemented by genetic and found in the Pantanal is a consequence of its recent ecophysiological studies. With these studies, it is possible emergence (Quaternary), with insufficient time for the to answer more precisely whether the characteristics speciation processes (Junk et al., 2006). described are merely phenotypic plasticity or if they are Although the term “Pantanal” refers to a region with the reflection of genetic changes. essentially hydrophyte vegetation, common in swamps, Extensive Pantanal floodable areas consist of xerophytic and mesophytic species are also distributed monodominant formations of tree populations. Among in various landscape units, with floristic composition them can be mentioned the areas of Tabebuia aurea influenced by phytogeographic provinces of Cerrado, (Manso) Benth.et Hook., locally known as paratudal, Amazon Rainforest, Semi-deciduous Forest and Chaco areas with Tabebuia heptaphylla (Vell.) Tol., known as (Damasceno-Junior et al., 2005; Oliveira, 2008). The piuval, the formation known as cambarazal comprised of

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Vochysia divergens Pohl, the lixeiral comprised of Curatella adverse condition for them. Palustrine species, aquatic americana L. and carandazal of Copernicia alba Morong macrophytes and, among these, amphibious species, are (Pott, 1994). It is noteworthy that these species are also exposed to favourable environmental conditions during distributed in plant communities of other biomes, but it is the rainy season, while they face environmental constraints only in the Pantanal that they form large monodominant during the dry season. populations of varying size and shape, reaching an area The Pantanal sensu lato areas, with less influence of flood of 1,000 hectares or more. These species maintain part of pulse, have flora temporarily subjected to environmental the shoot and root system in the anoxic environment for constraint, in this case, a lack of water. In high grassland periods ranging from 1 to 4 months. areas, the excess of light and shortage of water are extreme, The physical environmental characteristics are very especially in low rainfall months. During the annual cycle, distinct, when comparing the Pantanal, Cerrado and the plants located in floodable areas, such as those on Semi‑deciduous Forest. This makes the evaluation of species flood-free soils, are subjected to a significant deviation with wide distribution an interesting target for research. A from optimal conditions, and forced to change and respond recent work by Holsback-Menegucci et al. (2008) evaluated at various functional levels of the organism, which can young plants of Guazuma ulmifolia Lam. (Malvaceae) that characterise stress (Larcher, 2004). This condition is were artificially flooded for 100 days. These were from two reversible in principle, but it can become permanent and populations, one from the Paraná River Basin and the other irreversible. Stress implies a loss of vitality that worsens from the Pantanal. Higher growth and biomass of aerial with the duration of the event. portions were observed in the Pantanal plant population, A lack or excess of water in the environment leads to while hypertrophied lenticels were seen in the seedlings different kinds of situations. For example, plants subjected of the Paraná River Basin population, indicating distinct to a process of flooding are immediately exposed to a ecophysiological and morphoanatomical responses in decreased gas exchange, leading to anoxia or hypoxia both populations. conditions. This condition provokes restriction in breathing This may indicate that populations of the same in the root system, leading to inhibition of metabolic activity species occurring in vegetation formations with different and ATP production, restricting the supply of energy for abiotic selection pressure express distinct phenotypes in root growth and causing a reduction in plant development, ecophysiological terms, unaccompanied by differentiation which leads to morphological and/or physiological changes of the reproductive organ morphology, which is usually in the organisms, in order to obtain oxygen and energy used to characterise the species. This may be merely (Liao and Lin, 2001; Larcher, 2004). phenotypic plasticity or may be already genetically On the other hand, water is also the most common established. Santiago and Paoli (2007) pointed out that limiting factor for plant growth and its lack affects the large morphology variations in response to flood do not opening of the stomata, leading to reduction in photosynthetic determine the ecophysiological tolerance of the species capacity and growth rate, due to the restriction of gas to it, indicating that within a population, some individuals exchange. Additionally, as a drought tolerance mechanism, express morphological changes and others apparently do the stomata close during the period of highest water loss, not express any modification. coupled with reduced internal water potential of cells The visible changes in global climate have altered the through the accumulation of solutes that promote water frequency and intensity of drought and flooding events, absorption from the soil. These mechanisms allow the bringing important consequences for growth and survival of vegetation to survive in areas where fluid restriction is cultivated and native plants. Understanding what adaptations common (Larcher, 2004). allow plants to respond drought stress is crucial for predicting In this region, water stress suffered by different types the impacts of these climate changes in crop production of vegetation can be exemplified by paratudais, which are and environmental dynamics (Atkin and Macherel, 2009). subjected to water deficit during the drought period and Since almost all plant species that comprise the Pantanal anoxia of the root system during flood. This species has occur in other biomes whose physical environmental different strategies to cope with hydrological variation characteristics are distinct, populations of this biome are (Soares and Oliveira, 2009), but not all groups found excellent models for studies of adaptations to stress. in the Pantanal are capable of withstanding such water variations, leading to a sequence of colonisation processes. 2. Adaptations of the Plants of the Pantanal For example, areas previously occupied by species The plant communities of the Pantanal are annually adapted to high water supply conditions are occupied exposed to restrictions in obtaining resources. Thus, plants during periods of low rainfall by pioneer woody species growing in low areas of Pantanal wetlands, which are called that colonise previously flooded grassland. According Pantanal sensu stricto areas in this study, go through the to Pott (1994), species such as Curatella americana L annual cycle of excess and lack of water. Typical plants become dominant in sandy soils, while in clayey soil from flooded fields, riparian forests, shrubs, palustrine Tabebuia aurea takes over. However, when there is a plants and aquatic macrophytes are part of this community. series of rainy years, tree species like Vochysia divergens Some of these species are terrestrial, and flooding is an Pohl, Licania parvifolia Huber and Couepia uiti Benth.,

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 275-282 277 Scremin-Dias, E., Lorenz-Lemke, AP. and Oliveira, AKM. which are more tolerant to flooding, expand from patches for species composition, and may act as a filter for species of riparian vegetation (Pott and Pott, 2009). group. This relationship is barely known in the Pantanal; Many species do not have the ability to adapt to the in addition, the soil fertility also contributes to species soil flooding process, which in turn subjects their roots to distribution. For Wang et al. (2002), intermediate levels anoxic conditions, so they are indicators of the boundary of soil fertility tend to provide higher species richness in between floodable and dry areas. An example is the grasslands. Caraguatá (Bromelia balansae Mez), which defines areas The relation between flooding and species distribution that the flood waters reach during the rainy season. This in Pantanal grasslands is poorly known, few studies have condition is easily observed on the forest edge, where shown the species richness of these formations (Zeilhofer this species can survive and grow, because it is flood free. and Schessl, 1998; Pott and Adámoli, 1999). Periodic and Another interesting example can be observed in pulse-type flooding of the Pantanal’s low areas influences years of low flood, when Byrsonima orbignyana A. Juss. the morphological, anatomical and physiological responses (Malpighiaceae), which composes the monodominant (Scremin-Dias, 1999, 2000), and phenological and/or formations known as canjiqueirais, proliferates and colonises ethological adaptations, producing characteristic community periodically floodable grasslands. This species has all the structures that are not well known (Junk, 1999). morphoanatomical features of xerophytes: cuticle on leaf In low areas – Pantanal sensu stricto – where flooding is epidermis, hypodermis aquifer, vascular bundle hem, likely to be permanent, there is a predominance of aquatic hem extension lignified, and little intercellular space in species, which often turn into floating islands of vegetation chlorenchyma. The alternation of aquatic and terrestrial (baceiros). Pivari et al. (2008) conducted a study on the phases exposes the root system of this plant to complete dynamics of the floating islands formed by substrate histosol anoxia or hypoxia in a given period, which may mean with variable thickness, in the Pantanal sub-regions of deviation from the ecological optimum, and results in Miranda and Abobral. The species composition on these responses that suggest the existence of an adaptive traits baceiros is diverse and, depending on successional stage, complex, not only structural but also physiological. This shrubs and small trees can grow and reproduce on them. deviation is temporary, but for B. orbignyana, flooding Aquatic plants have different life forms (Pott and exposure for prolonged periods, much higher than the Pott, 2000; Scremin-Dias, 1999, 2009), distributed along annual seasonal pulse, implies a permanent injury, with the moisture gradient. These life forms range from free the death of the individuals. Thus, even in its natural floating through fixed floating, free submerged, fixed environment, this species is subject to optimum deviation, submerged, emergent, amphibious and emergent (Pott and and according to Larcher (2004), this can be interpreted as Pott, 2000; Scremin-Dias, 2009). They correspond to the a condition of stress, which is initially reversible, but can plant habit, reflecting the species’ tolerance to submergence become irreversible with the prolonged duration of a flood. or desiccation (Scremin-Dias, 2000), and are independent The flood pulse is an annual characteristic of the of the phylogenetic correlations between groups (Scremin- Pantanal, and presents alternated multi-annual cycles, Dias, 2009). some years with predominantly high inundation and A wide inventory conducted by Pott and Pott (2000) others with predominantly low inundation. This cycle found about 250 species of aquatic macrophytes in the shapes the landscape, “vanishing” the pioneer species Pantanal floodable areas, distributed among the phanerogams that are established in the floodable grasslands in low and cryptogams. Some aquatic macrophytes also form water years. However, this condition – death of species extensive monodominant areas, highlighting pirizal formed that are intolerant to extended flood periods – is also well by Cyperus giganteus Vahl, the caetezal with prevalence exemplified in Pantanal areas known as “arrombados of the Taquari River”. In this region, extensive areas of native of Thalia gemiculata L. and two species of native rice, vegetation have been destroyed by permanent flooding, Oryza glumaepatula Steud. and O. latifolia Desv., forming resulting in riparian forest death, caused by livestock and extensive rice fields along the Paraguay River. agriculture advancing into the high portion of this watershed Among these monodominant formations, Cyperus in recent decades. These activities have accelerated the giganteus and Thalia geniculata grow preferably in areas natural silting of the Taquari River, changing the riverbed with water level ranging up to 1.80 m at the flood peak, with and resulting in great losses of native vegetation areas water remaining in general for a short time at this level, (ANA, 2004). Interestingly, in the arrombados areas, subsequently decreasing gradually. These species tolerate terrestrial species intolerant of prolonged flooding have palustrine soils and flood-free areas, being denominated given way to hydrophytes, which colonise the extensive as amphibious. The amphibious way of life is the most wetlands permanently. peculiar one, because of the ecological amplitude of the species, which grow and can reproduce in both aquatic 3. Dynamics of Aquatic Plants in Relation to and flood-free (aerated soils) environments. Species with fixed floating, emergent and amphibious Seasonality habits generally have stems and roots attached to the One effect of the flood is to limit the number of species substrate. These underground parts may remain as resistance per environment (Rebellato and Cunha, 2005); duration, structures during the dry season (Scremin-Dias, 2009), levels and frequency of flooding are determining factors and display contractile roots that pull the apical buds

278 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 275-282 Adaptative strategies of plants to water stress below the soil surface, protecting them during the dry that have distinct morphoanatomical characteristics, linked season (Sculthorpe, 1967). This feature has already been to their adaptation to different habitats, taxonomic and described by Raunkiaer (1934) as acquired by higher plants evolutionary questions arise concerning the delimitation during the evolutionary process, with the aim of hiding of species. Molecular phylogenies using DNA sequences and protecting buds, allowing the survival of plants in may clarify aspects of the evolution of morphological and unfavourable environmental conditions. ecological traits, and the use of multiple genes describes Under these conditions, various plant species express these processes more accurately. The comparison of large phenotypic plasticity, an adaptation which, for Santiago homologous DNA sequences may be important in defining and Paoli (2007), cannot be mistaken for a mere character species of certain groups, because the observed coalescence expression in response to environmental pressures, but pattern and mutational events represent the genealogical should be considered as a process, which is not restricted relationships, tracing the history of the ancient DNA molecule only to the individual. According to these authors, the (Hewitt, 2001). Several types of molecular markers have organisms under these conditions may or may not express been used, making it possible to obtain a large amount of morphological, physiological or both traits, through gene data collected from small samples of biological material, activation or suppression, and these traits may or may not using non-destructive methods (Petit et al., 2001). have an adaptive component. Wu (2001) suggests that the most suitable genes to For amphibian species, established in flood-free soil investigate processes of species differentiation are those during the ebb, emergence of new stems, leaves and roots responsible for adaptive traits. Studies in this area assess may occur, and these characteristics of the tissues are phylogenetically related species or populations, in search very different from those observed in individuals of the of different alleles that have opposite effects on adaptive same species developed in water. Among the changes, value. Among the investigated genes, we can mention is important to highlight the significant decrease in the those related to reproduction, such as specific floral traits leaf sheet, the , the stem internodes, differential to different pollinator attraction (corolla color, position of distribution of stomata and increased lignification in the anthers and stigma, odor production) (Stuurman et al., 2004) vascular tissues as observed for various aquatic macrophytes and those related to adaptation to extreme environments in the Pantanal, accompanied by a seasonal cycle of flood (Brady et al., 2005). and drought (Scremin-Dias, 2000, 2009). Plants grown under different water regimes are good For some species that occur in periodically flooded areas, models for the study of resistance genes to excess and/or with intensely fluctuating water levels, ecophysiological scarcity of water. These plants have evolved under strong adaptations allow their “accommodation” to depth variations. selective pressure, with leaves emerged at certain times and This process, described by Ridge (1987), affords the submerged at others. These changes have a strong impact elongation of petioles, leaves, stem internodes, and floral on photosynthesis efficiency, and the genes linked to this scapes, shortly after the submersion of these organisms. function are strong candidates for differential adaptation. This, in response to anoxia, produces metabolites that Studying the rbcL gene, a chloroplast gene that encodes act on their cells, stretching or stimulating their division, a catalytic subunit of RuBisCO, in ecologically diverse resulting in an increase in length. Thus, the distribution aquatic plants, Iida et al. (2009) found positive selection in of species in areas with intense changes in water level some lines with heterophylly. This increase in the aminoacid favours the establishment of species that possess this substitution rate may imply a continuous adjustment of adaptive mechanism. RuBisCo over variable ecological conditions. To survive In the Pantanal, the vast native rice fields exemplify this and grow under anoxia conditions, some submerged process. Bertazzoni (2008) measured individuals of Oryza plants have to activate the transcriptional regulation of a latifolia with up to 5 m of stem elongation, after rising range of genes involved in physiological events that also waters. According to the author, the vegetative propagation control energy production, pH regulation and cell growth of this species is effective, because the branches drop on to (Harada et al., 2007). Other plants do not increase the the moist soil at the ebb period, allowing regrowth on the expression of genes that optimise photosynthesis under stem nodes, which stretch after the rainy season and form anoxia conditions, but rather the genes related to stem new individuals by budding or by seed germination. Oryza elongation and metabolism of different sugars to sustain glumaepatula also follows the water level by elongation of this growth (Das and Uchimiya, 2002; Harada et al., 2005). stem internodes, as observed by Silva (2010) over seasonal Tolerance of desiccation, as well as of water excess, induces cycles monitored in floodable fields of the Paraguay River. expression of specific genes, especially genes that cause coordinated cellular metabolism suppression. 4. The Evolutionary Significance of Differential Except for cultivated plant species, the genes directly Adaptations responsible for differential adaptation are rarely known. In these cases, molecular markers that represent selectively and Molecular studies have been increasingly used to evaluate adaptively neutral polymorphisms can be used (Durbin et al., adaptive differences of populations, distinguishing genetic 2003). Phylogeography, the study of spatial/temporal lineages and assessing whether or not they are associated distribution of genetic diversity, has been widely used with different environments. When comparing populations to assess the variability among individuals and between

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 275-282 279 Scremin-Dias, E., Lorenz-Lemke, AP. and Oliveira, AKM. related species (Avise, 2000). Through this approach it is CABIDO, M., Org. Caracterizacion ecologica y fitosociologica possible to identify independent evolutionary lineages and del Pantanal de Paiaguás. Mérida: CYTED/CIELAT. p. 197-201. associate (or not) them with certain geographic regions, Agência Nacional de Águas - ANA., 2004. Projeto Implementação an extremely useful tool to assess whether interpopulation de práticas de gerenciamento integrado de bacia hidrográfica para phenotypic differences reflect historical genetic divergence. o Pantanal e Bacia do Alto Paraguai. Subprojeto 1.7 – Solução DNA sequencing has wide applicability in these studies dos Problemas Relacionados aos “Arrombados” na Bacia do Rio because different parts of the genome have different rates of Taquari. Embrapa Pantanal. ANA/GEF/PNUMA/OEA. Available from: . evolution, making it possible to evaluate various taxonomic levels on several geographical scales (Avise, 2000). ALHO, CJR., 2008a. Biodiversity of the Pantanal: response to Among the most used markers in plant phylogeography seasonal flooding regime and to environmental degradation. Brazilian Journal of Biology, vol. 68, no. 4, p. 957-966. surveys, we can highlight the non-coding regions of plastid DNA (cpDNA) (Alsos et al., 2005), especially -, 2008b. The value of biodiversity. Brazilian Journal of Biology, those intergenic regions that tolerate mutations and vol. 68, no. 4, p. 1115-1118. evolve rapidly without affecting the function of adjacent ALHO, CJR. and GONÇALVES, UC., 2005. Biodiversidade do genes (Hamilton et al., 2003). The frequent uniparental Pantanal – Ecologia & Conservação. Campo Grande: UNIDERP. inheritance is one of the advantages of these markers in 144 p. differential assessment of pollen and seed flow (Hamilton ALSOS, IG., ENGELSKJON, T., GIELLY, L., TABERLET P. and Miller 2002); furthermore, the analysis of cpDNA and BROCHMANN, C., 2005. Impact of ice ages on circumpolar allows the identification of past hybridisation events that molecular diversity: insights from an ecological key species. are not detectable morphologically (Bleeker, 2003). As Molecular Ecology, vol. 14, no. 9, p. 2739-2753. the plastid genome is haploid, the effective population ARNHEIN, N., 1983. Concerted evolution of multigene families. size is smaller than when considering the nuclear genome. In: NEI, M. and KOEHN, RK., Ed. Evolution of genes and proteins. This feature speeds up the genetic drift processes; hence, Sunderland: Sinauer, p. 38-61. the cpDNA may show faster differentiation between ATKIN, OK. and MACHEREL, D., 2009. The crucial role of populations or divergent lineages (Hamilton et al., 2003). plant mitochondria in orchestrating drought tolerance. Annals of Among nuclear markers, ribosomal DNA (nrDNA) is Botany, vol. 103, no. 4, p. 581-597. widely studied in plants. The higher plants’ nrDNA is in AVISE, JC., 2000. Phylogeography: the history and formation of one or more chromosomal regions, and each arrangement species. London: Harvard University Press. 447 p. can display hundreds and even thousands of copies or BERTAZZONI, EC., 2008. Aspectos da biologia e fenologia de paralogs (Buckler-IV et al., 1997). Mutations in these Oryza latifolia Desv. (Poaceae) no Pantanal sul-mato-grossense. tandem repeats are individually homogenised through Campo Grande: Universidade Federal de Mato Grosso do Sul. concerted evolution, in which unequal crossing-over Dissertação de mestrado em biologia vegetal. and gene conversion are the main mechanisms involved BLEEKER, W., 2003. Hybridization and Rorippa austriaca (Arnhein, 1983). The mode and time of nrDNA concerted (Brassicaceae) invasion in Germany. Molecular Ecology, vol. 12, evolution varies greatly between different plant groups. no. 7, p. 1831-1841. Thus, nrDNA can present interspecific, interpopulation, and BRADY, KU., KRUCKEBERG, AR. and BRADSHAW Jr, HD., even intra-individual variation (Mayer and Soltis, 1999). 2005. Evolutionary ecology of plant adaptations to serpentine Populations with different morphoanatomical soils. Annual Review of Ecology, Evolution and Systematics, adaptations may reflect independent evolutionary units vol. 36, p. 243-266. and incipient speciation processes. They may be triggered BRASIL., 1999. Ações prioritárias para a conservação da by geographical, ecological, morphological or behavioral biodiversidade do Cerrado e Pantanal. Brasília: Ministério changes, with natural selection and genetic drift being do Meio Ambiente, FUNATURA, Conservation International, the most active evolutionary mechanisms. To understand Fundação Biodiversitas, Universidade de Brasília. 26 p. these processes and to distinguish phenotypic plasticity BUCKLER-IV, ES., IPPOLITO, A. and HOLTSFORD, TP., from genetic differentiation, it is interesting to approach 1997. The evolution of ribosomal DNA: divergent paralogues and the morphological characteristics in a genetic context, phylogenetic implications. Genetics, vol. 145, no. 3, p. 821-832. obtained through neutral or adaptive molecular markers. DAMASCENO-JUNIOR, GA., BEZERRA, MAO., BORTOLOTTO, Evaluating these patterns of several Pantanal species, we IM. and POTT, A., 1999. Aspectos florísticos e fitofisionômicos will be able to outline a more complete overview on the dos capões do Pantanal do Abobral. In Anais do II Simpósio sobre phytoecological evolution of this biome. Recursos Naturais e Socio-econômicos do Pantanal, Manejo e Conservação, Corumbá, 1996. Brasília: Embrapa. p. 203-214. References DAMASCENO-JUNIOR, GA., SEMIR, J., SANTOS, FAM. and LEITÃO-FILHO, HF., 2005. Structure, distribution of species ABDON, MM. and SILVA, JSV., 2006. Fisionomias da vegetação and inundation in a riparian forest of Rio Paraguai, Pantanal, nas sub-regiões do Pantanal Brasileiro. São José dos Campos: Brazil. Flora, vol. 200, no. 2, p. 119-135. INPE, Campinas: Embrapa Informática Agropecuária. 1 CD-ROM. DAS, A. and UCHIMIYA, H., 2002. Oxygen stress and adaptation ADÁMOLI, J. and POTT, A., 1996. Caracterizacion ecologica y of a semi-aquatic plant: rice (Oryza sativa). Journal of Plant fitosociologica del Pantanal de Paiaguás. In SARMIENTO, G. and Research, vol. 115, no. 5, p. 315-320.

280 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 275-282 Adaptative strategies of plants to water stress

DURBIN, ML., LUNDY, KE., MORREL, PL., TORRES- NA., Ed. A botânica no Brasil: pesquisa, ensino e políticas públicas MARTINEZ CL. and CLEGG, MT., 2003. Genes that determine ambientais. São Paulo: Sociedade Botânica do Brasil. p. 263-266. flower color: the role of regulatory changes in the evolution of phenotypic adaptations. Molecular Phylogenetics and Evolution, -, 2008. Pantanal – origens e características gerais. In OLIVEIRA, vol. 29, no. 3, p. 507-518. AKM., GARNÉS, SJA. and FAVERO, S., Ed. Meio ambiente e produção interdisciplinar: sociedade, natureza e desenvolvimento. ESTEVES, R., 2005. Uma nova espécie de Vernonia (Asteraceae) Campo Grande: Uniderp. p. 11-25. do Mato Grosso do Sul. Bradea, vol. 11, no. 1, p. 17- 28. PETIT, C., FRÉVILLE, H., MIGNOT, A., COLAS, B., RIBA, FAHN, A. and CUTLER, DF., 1992. Xerophytes. Berlin: Gebruder M., IMBERT, E., HURTREZ-BOUSSÉS, S., VIREVAIRE, Borntraeger. 176 p. M. and OLIVIERI, I., 2001. Gene flow and local adaptation in two endemic plant species. Biological Conservation, vol. 100, HAMILTON, MB. and MILLER, JR., 2002. Comparing relative no. 1, p. 21-34. rates of pollen and seed gene flow in the island model using nuclear and organelle measures of population structure. Genetics, PIVARI, MO., POTT, VJ. and POTT, A., 2008. Macrófitas aquáticas vol. 162, no. 4, p. 1897-1909. de ilhas flutuantes (baceiros) nas ilhas flutuantes (baceiros) nas sub-regiões do Abobral e Miranda, MS, Brasil. Acta Botanica HAMILTON, MB., BRAVERMAN, JM. and SORIA-HERNANZ, Brasilica, vol. 22, no. 2, p. 563-571. DF., 2003. Patterns and relative rates of nucleotide and insertion/deletion evolution at six chloroplast intergenic regions POTT, A., 1994. Ecossistema Pantanal. In: PUIGNAU, JP., Ed. in species of the Lecythidaceae. Molecular Biology Utilización y manejo de pastizales. Montevidéo: IICA-Procisur. and Evolution, vol. 20, no. 10, p. 1710-1721. p. 31-44. Diálogos, no. 40. HARADA, T., SATOH, S., YOSHIOKA, T. and ISHIZAWA, K., POTT, A. and ADAMOLI, J., 1996. Unidades de vegetação 2005. Expression of sucrose synthase genes involved in enhanced do Pantanal dos Paiaguás. In Anais do II Simpósio sobre elongation of pondweed (Potamogeton distinctus) turions under Recursos Naturais e Sócio-Econômicos do Pantanal. Corumbá: anoxia. Annals of Botany, vol. 96, no. 4, p. 683-692. CPAP‑EMBRAPA, UFMS. p. 183-202. -, 2007. Anoxia-enhanced expression of genes isolated by suppression -, 1999. Unidades de vegetação do Pantanal dos Paiaguás. In Anais subtractive hybridization from pondweed (Potamogeton distinctus do II simpósio sobre recursos naturais e sócio-econômicos do A. Benn.) turions. Planta, vol. 226, no. 4, p. 1041-1052. Pantanal: manejo e conservação. Corumbá: Embrapa Pantanal. HEWITT, GM., 2001. Speciation, hybrid zones and phylogeography p. 183-202 – or seeing genes in space and time. Molecular Ecology, vol. 10, POTT, A., SILVA, JSV., SALIS, SM., POTT, VJ. and SILVA, no. 3, p. 537-549. MP., 2000. Vegetação e uso da terra. In SILVA, JSV., Org. HOLSBACK-MENEGUCCI, ZR., SCREMIN-DIAS, E. and Zoneamento ambiental, Borda Oeste do Pantanal: Maciço do SANTIAGO, EF., 2008. Estudo comparativo de respostas ao Urucum e adjacências. Brasília: Embrapa. p. 111-131. alagamento em plantas jovens de espécies arbóreas provenientes POTT, VJ. and POTT, A., 2000. Plantas aquáticas do Pantanal. do pantanal, Mato Grosso do Sul, Brasil. Campo Grande: Brasília: Embrapa. Corumbá/MS. 404 p. Universidade Federal de Mato Grosso do Sul. Dissertação de mestrado em biologia vegetal. -, 2009. Vegetação do Pantanal: fitogeografia e dinâmica. In Anais II Simpósio de Geotecnologias no Pantanal. Corumbá: Embrapa IIDA, S., MIYAGI, A., AOKI, S., ITO, M., KADONO, Y. Informática Agropecuária/INPE. p. 1065-1076. and KOSUGE, K., 2009. Molecular adaptation of rbcL in the heterophyllous aquatic plant Potamogeton. PLoS One, vol. 4, REBELLATO, L. and CUNHA, CN., 2005. Efeito do “fluxo no. 2, p.e4633. sazonal mínimo da inundação de um campo inundável no Pantanal de Poconé, MT, Brasil”. Acta Botanica Brasilica, vol. 19, no. 4, JUNK, WJ., 1999. O conceito de pulso de inundação e suas p. 789-799. implicações para o Pantanal de Mato Grosso. In Anais do II simpósio sobre recursos naturais e sócio-econômicos do Pantanal: RIDGE, I., 1987. Ethylene and growth control in amphibious plants. manejo e conservação. Corumbá: Embrapa Pantanal. p. 17-28. In CRAWFORD, RMM., Ed. Plant life in aquatic and amphibious habitats. Oxford: Blackwell Scientific Publications. p. 53-76. JUNK, WJ., NUNES DA CUNHA, C., WANTZEN, KM., PETERMANNN, P., STRÜSSMANN, C., MARQUES, MI. and SANTIAGO, EF. and PAOLI, AAS., 2007. Respostas morfológicas ADIS, J., 2006. Biodiversity and its conservation in the Pantanal em Guibourtia hymenifolia (Moric.) J. Leonard (Fabaceae) e of Mato Grosso, Brazil. Aquatic Sciences, vol. 68, no. 3, p. 1- 32. Genipa americana L. (Rubiaceae), submetidas ao estresse por deficiência nutricional e alagamento do substrato. Revista Brasileira LARCHER, W., 2004. Ecofiosiologia vegetal. São Carlos: de Botânica, vol. 30, no. 1, p. 129-138. RiMa. 531 p. SCREMIN-DIAS, E., 1999. O retorno à origem aquática. In: LIAO, CT. and LIN, CH., 2001. Physiological adaptation of crop SCREMIN-DIAS, E., POTT, VJ., SOUZA, PR. and HORA, RC. plants to flooding stress. Proceedings of the National Science Nos Jardins Submersos da Bodoquena: guia para identificação Council, vol. 25, no. 3, p. 148-157. de plantas aquáticas de Bonito. Campo Grande: UFMS. p. 25-41 MAYER, MS. and SOLTIS, PS., 1999. Intraspecific phylogeny -, 2000. A plasticidade fenotípica das macrófitas aquáticas em analysis using ITS sequences: insights from studies of the resposta à dinâmica ambiental. In CAVALCANTI, TC. and Streptanthus glandulosus complex (Cruciferae). Systematic WALTER, BMT., Org. Tópicos atuais em botânica: palestras Botany, vol. 24, no. 1, p. 47-61. convidadas do 51º Congresso Nacional de Botânica. Brasília: OLIVEIRA, AKM., 2007. Pantanal – alguns parâmetros físico- Embrapa Recursos Genéticos e Biotecnologia/Sociedade Botânica químicos e biológicos. In BARBOSA, LM and SANTOS JUNIOR, do Brasil. p. 189-193.

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 275-282 281 Scremin-Dias, E., Lorenz-Lemke, AP. and Oliveira, AKM.

-, 2009. Tropical aquatic plants: morphoanatomical adaptations. In STUURMAN, J., HOBALLAH, ME., BROGER, L., MOORE, DEL-CLARO, K. and RICO-GRAY, Org. Encyclopedia of tropical J., BASTEN, C. and KUHLEMEIER, C., 2004. Dissection of biology and conservation management. Paris: UNESCO/EOLSS. floral pollination syndromes in Petunia. Genetics, vol. 168, vol. 1, p. 84-132. no. 3, p. 1585-1599. SCULTHORPE, CD., 1967. The Biology of aquatic vascular WANG, G., ZHOU, G., YANG, L. and LI, Z., 2002. Distribution, plants. London: Eduard Arnold Publ. 610 p. species diversity and life-form spectra of plant communities along an altitudinal gradient in the northern slops of Qilianshan SILVA, RH., 2010. Dinâmica e estrutura de comunidades em área Mountains, Gansu, China. Plant Ecology, vol. 165, no. 2, p. 169-181. de campos com inundação sazonal na sub-região do Pantanal do rio Paraguai, Corumbá, MS. Campo Grande: Universidade WU, C-I., 2001. The genic view of the process of speciation. Federal de Mato Grosso do Sul. Dissertação de mestrado em Journal of Evolutionary Biology, vol. 14, no. 6, p. 851-865. biologia vegetal. ZEILHOFER, P. and SCHESSL, M., 1998. Relationship between SOARES, JJ. and OLIVEIRA, AKM., 2009. O paratudal do vegetation and environmental conditions in the northern Pantanal Pantanal de Miranda, Corumbá-MS, Brasil. Revista Árvore, of Mato Grosso, Brazil. Journal of Biogeography, vol. 27, no. 1, vol. 33, no. 2, p. 339-347. p. 159-168.

282 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 275-282 Ethnobotany and traditional medicine of the inhabitants of the Pantanal Negro sub-region and the raizeiros of Miranda and Aquidauna, Mato Grosso do Sul, Brazil Oliveira, AKM.*, Oliveira, NA., Resende, UM. and Martins, PFRB. Programa de Pós-graduação em Meio Ambiente e Desenvolvimento Regional, Universidade Anhanguera – Uniderp, Rua Alexandre Herculano, 1400, Jardim Veraneio, CEP 79037-280, Campo Grande, MS, Brazil *e-mail: [email protected] Received October 14, 2010 – Accepted December 13, 2010 – Distributed April 30, 2011 (With 1 figure)

Abstract A survey on the use of medical plants was carried out in the rural communities of the Rio Negro sub-region of the Pantanal and the raizeiros from Aquidauana and Miranda municipalities, Mato Grosso do Sul, Brazil, in order to recover the ethnobotanical and ethnopharmacological knowledge of these communities. Structured questionnaires were run with the residents of eight farms and 12 raizeiros. The results reveal 25 botanical families, 45 genera and 48 species of medicinal plants used, six of which are indicated for kidney disturbances, six for urinary disturbances, five for inflammation treatment, 13 for stomach aches, 10 for respiratory disturbances, four for treating sprains, four for healing wounds, four as anti-diarrheaic and one as antipyretic, among other illnesses. The main family was Asteraceae, with 12 species used. The principal preparation methods of the medicinal herbs in the Rio Negro sub‑region and surrounding areas were infusion (35) and, mostly, mixed with “chimarrão” or “mate quente”, traditional beverage. Nineteen exotic species are used by the raizeiros, (39.58%), which indicates a strong influence of the urban environment. The traditional pantaneiros have greater knowledge of medicinal plants than the raizeiros, and they cited only five exotic species (16.1%). Keywords: folk medicine, medicinal plants, ethnopharmacology.

Etnobotânica e medicina tradicional dos habitantes da sub-região do Pantanal do Negro e raizeiros das cidades de Miranda e Aquidauana, Mato Grosso do Sul, Brasil

Resumo Foi realizado um levantamento sobre o uso de plantas medicinais junto às comunidades rurais, da sub-região do Rio Negro e raizeiros das cidades de Aquidauana e Miranda, Mato Grosso do Sul, Brasil. O objetivo foi resgatar o conhecimento etnobotânico e etnofarmacológico dessas comunidades, por meio da aplicação de questionários a moradores de oito fazendas e 12 raizeiros. Os resultados indicaram a utilização de 25 famílias, 45 gêneros e 48 espécies de plantas medicinais, sendo seis utilizadas para afecções dos rins, seis para tratamento das vias urinárias, cinco no tratamento de inflamações, 13 para dores estomacais, quatro como cicatrizantes, 10 para afecções do aparelho respiratório, quatro para todo o tipo de torções, quatro como antidiarreicas e uma no combate às febres, entre outras doenças. A principal família utilizada é Asteraceae, com 12 espécies. As principais formas de utilização das plantas são os chás por infusão (citado 35 vezes), isoladamente ou com as partes da planta misturadas no mate quente ou chimarrão, bebidas tradicionais da região pantaneira. O número de espécies exóticas utilizadas, 19 (39,58%), indica forte influência das correntes migratórias para a região, o que pode comprometer a médio e longo prazos, o conhecimento das populações locais. Os pantaneiros tradicionais têm maior conhecimento sobre as plantas medicinais nativas do que os raizeiros das cidades de Miranda e Aquidauna, citando apenas cinco espécies exóticas (16,1%). Palavras-chave: medicina popular, plantas medicinais, etnofarmacologia.

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1. Introduction Thus, this biome is an important vegetation complex for the study of medicinal herbs, covering a diversity of The use of plants in the treatment of several diseases species with great potential for ethnobotanical studies (e.g. is reported in different populations (e.g., Berg and Silva, Conceição and Paula, 1986; Pott and Pott, 1994; Bortolotto, 1988; Bird, 1991; Verger, 1995; Guarim-Neto, 2006; 1999; Souza and Guarim-Neto, 1999; Pott and Pott, 2000; Kunwar et al., 2006). The knowledge of medicinal plants Schwenk and Silva, 2000; Campos Filho, 2002). It is often represents the only therapeutic option for many also occupied by a native population with great cultural communities and ethnic groups. Revene et al. (2008) importance, adapted to the intermittent cycles of flood and point out that traditional medicine in poor countries is drought of the region, the pantaneiros or marsh‑dwellers the most accessible practice and, in certain situations, the (Nogueira, 2002). only treatment available. According to Maciel et al. (2002), the use of plants The use of plants for therapeutic purposes in the to treat and cure diseases is as old as the human species Pantanal region has long been reported in various Indian and today in the poorest regions of the country and even tribes. Since the first colonisation of the region, especially on the outskirts of large Brazilian cities, medicinal plants during the Paraguay War (1864-1870), extractivist activities are sold in street markets and fairs and found in the have been intensified in other communities and are now backyards of residences. The World Health Organization part of the ‘pantaneiros’ lives, either for medicinal ends or (WHO) states that approximately 80% of the population just to bring comfort in the face of their daily adversities use traditional medicine in primary health care (WHO, (WHO, 2002). 2002). The discovery and disclosure of medicinal flora The knowledge of the correct use of plant species properties, through the knowledge of traditional populations, normally belongs to restricted groups of the population, is, therefore, an important tool in preserving the cultural known as raizeiros (generally people with little formal richness of different regions. education, who through the knowledge transmitted by In Brazil, the use of herbs for medicinal purposes is their parents or other people with empirical knowledge, a widespread practice, enhanced by cultural differences, use plants for disease treatment), benzedeiras (usually deriving from colonisation by the European and African women, who treat distinct diseases through prayer and populations, in addition to traditional indigenous knowledge herbs) and other, usually elderly, people, who received (Gomes et al., 2008). According to Martins et al. (2000), medicinal information from their ancestors (Guarim-Neto, the use of plants to treat diseases has, fundamentally, 2006). As these groups are restricted and often threatened influences from several different cultures that include the by environmental changes, which alter their lifestyle and Indians who use phytotherapy in a mystical way: the shaman culture, the recovery of this ethnobotanical knowledge is or witch doctor of the tribe often uses herbs with narcotic fundamental in rescuing traditions that may soon be lost. and/or hallucinogenic effects to dream about spirits. These Considering the information gaps in the ethnobotanical reveal the herb or the procedure to be followed to cure the and ethnopharmacological knowledge of the traditional sick person, or the shaman may observe animals that look pantaneiros from Rio Negro sub-region and the raizeiros for certain plants when they are sick. Black populations of the municipalities of Aquidauana and Miranda, this descended from African slaves have also introduced new work aims to identify the plants used in folk medicine species with curative intent, seeking to “expel” the disease and their respective utilisation. through rituals and natural products, including those of animal origin. 2. Material and Methods This mixture of traditions, associated with the high plant diversity in Brazil, has led to a traditional medicine This study was conducted with 14 traditional residents based on different plants and methods of treatment and of eight farms (Santa Emilia, Chão Parado, Conquista, researchers (e.g., such as Correa, 1926-1978; Rizzini Santa Maria, Campo Lourdes, São Roque, Bandeirantes and Mors, 1976; Berg, 1993; Ming, 1995; Agra, 1996) and Santa Marta) near the city of Aquidauana, and with demonstrate the richness of medicinal flora in different twelve raizeiros, six from the urban area of Aquidauana Brazilian regions. and six of Miranda municipalities, located at the edge of the Among the Brazilian biomes, the Pantanal is a region southern Pantanal, Mato Grosso do Sul, Brazil (Figure 1). with associated vegetation formations and, according to These towns are directly influenced by the Pantanal Pott and Pott (1994), the colonisation of species from region. They have a large rural-origin population and, for regions like Chaco, Cerrado, Amazon and Atlantic forest this reason, were chosen to be the interview set. has allowed the occurrence of wide distribution species A structured questionnaire (popular name, preparation and low endemism. Alho (2008a,b) and Oliveira (2007, method and therapeutic indications) was developed and 2008) affirm that each sub-region of Pantanal wetland applied in march-october/2008, in order to define a profile (a periodically flooded area), shows vegetation characteristics of the traditional pantaneiros and raizeiros, concerning associated with different environmental factors such as their experience and knowledge of the therapeutic usage of soil type, flood level and slope, which influence species medicinal plants. The species cited by Sano and Almeida distribution and provide great floristic diversity. (1998) and Pott and Pott (1994, 1999) were considered

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Figure 1. Map of the Pantanal wetland, showing the 10 subregions, by Hamilton et al. (1996).

native to the region, and Lorenzi and Matos (2002) were herbarium for identification and deposit. The classification also consulted. system used was APG II (Angiosperm Phylogeny Group, 2003). In this study, the interviews were designed for people born in the Pantanal region or who have spent most of their 3. Results and Discussion lives in the region, and interacted with the environment In the present study 25 families, 45 genera and 48 species through the use of natural resources as a way of survival. of medicinal plants of routine use were identified, 19 of To avoid embarrassment, the interviewees were free to which were exotic species (introduced in the region) and speak according to their own situation and the interviews 29 (60.42%) were native (Table 1). The family with largest were carried out using regional language. number of used species was Asteraceae (12), followed by The species mentioned by the pantaneiros and raizeiros the family Lamiaceae (7). were collected in the indicated areas by the interviewees, The herb “boldo” (P. barbatus), an introduced species, and transported to the Anhanguera-Uniderp University was the most cited (seven times), which indicates the strong

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Table 1. Family, popular and scientific name, citation number (CN) – “Pantaneiros” (P) and “raizeiros” (R), preparation method (PM), therapeutic indications (TI) and origin of the medicinal plants cited by the raizeiros of the municipalities of Aquidauana and Miranda and by the traditional pantaneiros of the Rio Negro sub-region, Pantanal, Mato Grosso do Sul, Brazil. Native Family Popular and scientific name CN PM TI species Adoxaceae Sabugueiro - Sambucus australis 1 - P Infusion Measles and fever Yes Cham. & Schltdl. Amaranthaceae Terramicina, Chapéu de couro 1 - R Poultice (2) Wounds (2) Yes (Cabeça-branca), Estomalina - 1 - P Infusion (1) Stomach aches (1) Alternanthera brasiliana (L.) O. Kuntze Erva-de-Santa Maria ou mastruz - 3 - R Smoothie Vermifuge Yes Chenopodium ambrosioides L. 2 – P Arecaceae Coco da Bahia - Cocos nucifera L. R - 1 Infusion Hepatitis No

Asteraceae Anador - Artemisia verlotorum 2 - R Infusion Pains Yes Lamotte 2 - P Chifre-de-carneiro - 1 - R Infusion Diuretic/ Yes Acanthospermum hispidum DC. 1 - P kidney disturbances Picão - Bidens pilosa L. 2 - R Infusion Verminosis Yes 1 - P Arnica - Lychnophora ericoides 2 - R Poultice Healing/ Yes Mart. 1 - P Pains Caferana - Vernonia polyanthes 1 - P Infusion Stomach aches Yes Less. Guaco - Mikania laevigata Schultz 1 - R Infusion Cough Yes Bip. ex Baker Camomila - Chamomilla recutita 1 - R Infusion Colic and sedative No (L.) Rauschter Cravo-de-defunto - Tagetes patula 1 - R Infusion Pneumonia No L. Carqueja - Baccharis articulata 1 - R Infusion Stomach aches Yes (Lam.) Pers. Assa-peixe – Vernonia ferruginea 1 - P Infusion Cough/ Yes Less. Snoring Erva de Luceira - Pluchea sagittalis 2 - R Poultice Wounds/ Yes ( Lam.) Cabrera 1 - P Sprains Bignoniaceae Piúva - Tabebuia heptaphylla (Vell.) 1 - P Infusion Inflammation Yes Tol. Paratudo, Ipê - T. aurea (Manso) 1 - R Decoction (1) Bronchitis/ Yes Benth. & Hook. f. ex. S. Moore 2 - P Infusion (2) Inflammationand several different ailments Stomach Celastraceae Cancorosa - Maytenus cf. 1 - P Infusion Infection Yes macrodonta Reiss. Crassulaceae Saião - Kalanchoe brasiliensis 1 - P Chew the leaf Stomach aches No Camb. Curcubitaceae Melão-de-São-Caetano - Momordica 1 - P Poultice Healing No charantia L. Euphorbiaceae Quebra-pedra - Phyllanthus amarus 1 - R Infusion Kidney stones Yes K. Schum. 2 - P

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Table1. Continued... Native Family Popular and scientific name CN PM TI species Fabaceae Fedegoso - Senna occidentalis (L.) 1 - R Cold tea Stimulant/ Yes Link 3 - P Verminosis Amargoso - Vatairea macrocarpa 1 - P Infusion Stomach/ Yes (Benth.) Ducke. Liver Lamiaceae Boldo - Plectranthus barbatus Andr. 4 - R Maceration/ Digestion No 3 - P Cold tea Boldo (Boldo do Chile) - 1 - P Infusion Head and stomach No P. neochilus Schlechter aches Erva cidreira - Melissa officinalisL. 2 - R Infusion High pressure and No 1 - P insomnia

Poejo - Mentha pulegium L. 2 - R Infusion Flu No Hortelã do campo - Hyptis crenata 1 - R Infusion Vermifuge Yes Pohl ex Benth. Alecrim - Rosmarinus officinalisL. 2 - R Infusion Heart disturbances No

Hortelã gorda - Mentha x piperita L. 1 - P Infusion Stomach aches No Lauraceae Abacateiro - Persea americana Mill. 1 - R Infusion Urinary disturbances No Lytraceae Romã - Punica granatum L. 1 - R Infusion Gastritis No Malvaceae Malva branca - Waltheria communis 2 - P Infusion Wound asepsis Yes A. St.-Hil. Nyctaginaceae Amarra-pinto - Boerhavia diffusa L. 1 - R Infusion Infection/ Yes Diuretic Piperaceae Pariparoba - Piper regnellii (Miq) 2 - P Infusion Stomach Yes C. DC. Plantaginaceae Vassourinha - Scoparia 2 - P Infusion Renal pains Yes montevidensis (Spreng.) R. E. Fries Poaceae Capim amargoso - Setaria 1 - P Poultice Healing Yes poiretiana (Schult.) Kunth. Capim cidreira - Cymbopogon 1 - R Infusion Sedative No citratus (D.C.) Stapf 1 - P Polygonaceae Erva-de-bicho - Polygonum 1 - P Poultice Wound asepsis/ Yes hydropiperoides Michx. Chilblain Rubiaceae Congonha de bugre - Rudgea 2 - P Infusion Heart disturbances/ Yes viburnoides (Cham.) Benth. kidney Rutaceae Arruda - Ruta graveolens L. 1 - R Infusion Menstrual colic pains No Laranjeira - Citrus aurantium var. 1 - R Infusion Pains/ flu No Dalmau Solanaceae Beladona - Atropa belladonna L. 1 - R Hot Poultice Twist pains No Juá - Solanum viarum Dun. 1 - R Infusion Kidney Yes 2 - P Tomate cereja - Solanum 1 - R Maceration/ Kidney disturbances No lycopersicon L. Cold Tea Teophrastaceae Erva de bugre - Clavija nutans 1 - P Infusion Flu Yes (Vell.) Stahl. Verbenaceae Gervão - Stachytarpheta 1 - R Ointment Healing Yes cayennensis (Rich.) Vahl 1 - P Xanthorrhoeaceae Babosa - Aloe arborescens Mill. 1 - R Hot poultice Pneumonia No

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 283-289 287 Oliveira, AKM. et al. influence of exotic species on the local culture. Successively, species “boldo” (P. barbatus) was the most mentioned; the most remembered herbs were “erva-de-santa Maria” or this species is indicated for stomach aches and as digestive “mastruz” (C. ambrosioides) (5), “anador” (A. vermolotorum) stimulant, similar results found by Guarim-Neto (1984) and “fedegoso” (S. occidentalis) (4), “juá” (S. viarum), and Berg (1980). According to Costa et al. (2003), studies “picão” (B. pilosa), “arnica” (L. ericoides), “quebra-pedra” revealed that “boldo” has hypotensive, vasodilation, gastric (P. amarus) and “erva cidreira” (M. officinalis) (3). hyposecretory, blood pressure reducing anti-dyspeptic Most of the interviewees (35-71.4%) carry out infusion properties. The second most cited species was “erva-de-Santa preparations with the herbs, pouring hot water over selected Maria” (C. ambrosioides) (native), used as a vermifuge. parts of them and letting them steep for a few minutes. The medicinal use of this species is widespread, showing The medicinal herbs can be also added to “chimarrão” or stomachic, anti-rheumatic and anthelmintic properties. “mate-quente”, a traditional hot beverage prepared from “Alecrim” (R. officinalis), “anador” (A. vermolotorum), steeping dried leaves of Ilex paraguariensis A. St.-Hil. “arnica” (L. ericoides), “capim cidreira” (C. citratus), This hot beverage is normally drunk when neighbours or “picão” (B. pilosa) and “poejo” (M. pulegium) were friends gather in the early morning or late afternoon to mentioned three times; they are all commonly used in folk talk about daily issues, forming a particular social setting medicine, except for “arnica” (Lorenzi and Matos, 2002). known as “rodas de prosa”. The others species were cited only once. The latter method is commonly used by the population, Regarding the answers of traditional pantaneiros, due to easy handling of the medicinal plants, uniting the 31 medicinal species were cited (Table 1), with only five traditional habit of drinking “chimarrão” with the necessity exotic ones (16.1%), indicating a strong link with the local of treating the sick. flora and little external influence on medicinal herb use. The use of medicinal herbs in the states of Mato Grosso “Boldo” also shows a higher frequency of citations and Mato Grosso do Sul is reported by different researchers. (three), together with “fedegoso” (S. occidentalis), used Berg (1980) conducted a study in the cities of Cuiabá in phytotherapy as a stimulant, vermifuge and against and Chapada dos Guimarães, Mato Grosso, and reported anemia. The literature demonstrates that organic extracts 103 species used for medicinal purposes. Guarim-Neto of S. occidentalis have purgative, hepatic, antibacterial, (2006), in a compilation of his earlier research, reveals that antipyretic, antitumor, expectorant, anti-inflammatory, 56 medicinal plants are used in the traditional medicine diuretic, antifungal and neurotoxic properties for cattle practices of pantaneiros, eight more than those reported (Viegas et al., 2006). The species with only two citations for the Rio Negro sub-region. were “anador” (A. vermolotorum), “congonha de bugre” Berg and Silva (1988) performed a survey in the cities (R. viburnoides), “erva-de-Santa Maria” (C. ambrosioides), of Campo Grande, Aquidauana and Miranda, and in the “juá” (S. viarum), “malva branca” (W. communis), “paratudo” Pantanal of Mato Grosso do Sul State, in which they listed (T. aurea), “pariparoba” (P. regnellii), “quebra-pedra” 104 species considered as medicinal flora. Compared with (P. amarus) and “vassourinha” (S. montevidensis), commonly the data obtained in the present study, 41 species identified used in Brazilian folk medicine (Lorenzi and Matos, 2002; in this research were not reported by Berg and Silva (1988). Guarim-Neto, 2006). The Aquidauana and Miranda raizeiros named There are 13 species common to both localities, such 33 species, 16 of them exotic (Table 1), such as “abacateiro” as “anador” (A. vermolotorum), “arnica” (L. ericoides), (P. americana), “boldo” (P. barbatus), “erva cidreira” “boldo” (P. barbatus), “capim cidreira” (C. citratus), (M. officinalis), “erva-de-Santa Maria” (C. ambrosioides), “juá” (S. viarum), “picão” (B. pilosa) and others, with “picão” (B. pilosa), “romã” (P. granatum), among others. the smallest portion of exotic species (4-30.8%). The The information obtained indicates that raizeiros traditional pantaneiros apparently have a greater knowledge interviewed are former residents of rural areas, who moved of native medicinal plants than the raizeiros (residents of to the towns to seek a better life. However, they still keep urban areas), who mentioned a representative number of up rural customs, cultivating herbs in the backyard, even exotic plants. when living close to pharmacies. These recent urban The knowledge of native plants is getting lost in residents utilise natural medicine routinely, and share their the Pantanal region, due to neglect of the ‘pantaneiros’ vast knowledge of medicinal herbs with neighbours and traditional values, their migration to urban areas and close relatives. However, it was observed that the longer contact with new immigrants arriving in the region. they had lived in the town, the greater was the difficulty The recovery of this empirical knowledge is important to list a significant number of species that had been used for biodiversity conservation, to create alternatives for in their previous rural life. subsistence livelihoods and to maintain cultural diversity. Furthermore, 39.58% of the species mentioned by the Acknowledgements – We are indebted to Anhanguera-Uniderp raizeiros are exotic, which indicates the strong influence University, which supported this work (Interdisciplinary Group of the urban environment on the utilisation of medicinal of Research - GIP Project) and provided a scholarship. And also flora and the gradual loss of any connection with the to the referees, for their anonymous work of corrections and rural environment and its medicinal species. The exotic suggestions.

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References study from Dolpa, Humla, Jumla and Mustang districts of Nepal. Journal of Ethnobiology and Ethnomedicine, vol. 2, no. 27, 6 p. AGRA, MF., 1996. Plantas da medicina popular dos Cariris LORENZI, H. and MATOS, FJA., 2002. Plantas medicinais no Velhos (Paraíba, Brasil): espécies mais comuns. João Pessoa: Brasil: nativas e exóticas. Nova Odessa: Instituto Plantarum. 512 p. União. 112 p. MACIEL, MAM., PINTO, AC. and VEIGA JUNIOR, VF., 2002. ALHO, CJR., 2008a. Biodiversity of the Pantanal: response to Plantas medicinais: a necessidade de estudos multidisciplinares. seasonal flooding regime and to environmental degradation. Química Nova, vol. 25, no. 3, p. 429-438. Brazilian Journal of Biology, vol. 68, no. 4, p. 957-966. MARTINS, ER., CASTRO, DM., CASTELLANI, DC. and DIAS, -, 2008b. The value of biodiversity. Brazilian Journal of Biology, JE., 2000. Plantas medicinais. Viçosa: Editora Universidade vol. 68, no. 4, p. 1115-1118. Federal de Viçosa. 220 p. Angiosperm Phylogeny Group - APG II, 2003. An update of MING, LC., 1995. Levantamento de plantas medicinais na Reserva the angiosperm phylogeny group classification of the orders and Extrativista “Chico Mendes” – Acre. Botucatu: Universidade families of flowering plants: APGII. Botanical Journal of the Estadual de São Paulo. Tese de Doutorado. Linnean Society, vol. 141, no. 4, p. 399-436. NOGUEIRA, AX., 2002. Pantanal: homem e cultura. Campo BERG, ME van den., 1980. Contribuição à flora medicinal do Grande: UFMS. 156 p. Estado de Mato Grosso. Ciência e Cultura, vol. 33, p. 163-170. Suplemento. OLIVEIRA, AKM., 2007. Pantanal – alguns parâmetros físico- químicos e biológicos. In BARBOSA, LM. and SANTOS JUNIOR, BERG, ME. van den and SILVA, MHL., 1988. Contribuição à NA., Ed. A botânica no Brasil: pesquisa, ensino e políticas públicas flora medicinal de Mato Grosso do Sul. Acta Amazonica, vol. 18, ambientais. São Paulo: Sociedade Botânica do Brasil. p. 263-266. no. 1-2, p. 9-22. Suplemento. -, 2008. Pantanal – origens e características gerais. In OLIVEIRA, -, 1993. Plantas medicinais da Amazônia: contribuição ao seu AKM., GARNÉS, SJA. and FAVERO, S., Ed. Meio ambiente e conhecimento sistemático. Belém: CNPq/MPEG. 206 p. produção interdisciplinar: sociedade, natureza e desenvolvimento. BIRD, C., 1991. Medicines from the rainforest. New Scientist, Campo Grande: Uniderp, p. 11-25. vol. 17, p. 34-39. POTT, A. and POTT, VJ., 1994. Plantas do pantanal. Brasília: BORTOLOTTO, IM., 1999. Educação e uso de recursos naturais: EMBRAPA, 320 p. um estudo na comunidade de Albuquerque, Corumbá, Mato Grosso do Sul, Pantanal. Cuiabá: Universidade Federal de Mato -, 1999. Flora do Pantanal – listagem atual de fanerógamas. In Grosso. Dissertação de mestrado. Anais do Simpósio sobre Recursos Naturais e Sócio-Econômicos do Pantanal, Manejo e Conservação, 2, 1996. Corumbá: Embrapa CAMPOS FILHO, LVS., 2002. Tradição e ruptura: cultura e Pantanal. p. 297-325. ambiente pantaneiros. Cuiabá: Entrelinhas, 180 p. POTT, VJ. and POTT, A., 2000. Plantas CONCEIÇÃO, CA. and PAULA, JE., 1986. Contribuição para o aquáticas do Pantanal. Brasília: Embrapa conhecimento da flora do Pantanal mato-grossense e sua relação Comunicação para Transferência de Tecnologia. 404 p. com a fauna e o homem. In Anais do I Simpósio sobre Recursos Naturais e Sócio-Econômicos do Pantanal, Corumbá. Brasília: REVENE, Z., BUSSMANN, RW. and SHARON, D., 2008. Embrapa DDT. p. 107-130. From Sierra to Coast: Tracing the supply of medicinal plants in Northern – A plant collector’s tale. Ethnobotany Research CORRÊA, MP. 1926-1978. Dicionário das plantas úteis do Brasil & Applications, vol. 6, p. 15-22. e exóticas cultivadas. Rio de Janeiro: Ministério da Agricultura, Indústria e Comércio. 6 volumes. RIZZINI, CT. and MORS, WB., 1976. Botânica econômica brasileira. São Paulo: EPU/EDUSP. 207 p. COSTA, MCCD., AGUIAR, JS. and NASCIMENTO, SC., 2003. Atividade citotóxica de Plectranthus barbatus. Acta Farmacéutica SANO, SM. and ALMEIDA, SM., 1998. Cerrado: ambiente e Bonaerense, vol. 22, no. 2, p. 155-158. flora. Planaltina: Embrapa-CPAC. 556 p. GOMES, HHS., DANTAS, IC. and CATÃO, MHCV. 2008. SCHWENK, LM. and SILVA, CJ., 2000. A etnobotânica da morraria Plantas medicinais: sua utilização nos terreiros de umbanda e Mimoso no Pantanal de Mato Grosso. In Anais do III Simpósio candoblé na zona leste de cidade de Campina Grande-Pb. BioFar, sobre Recursos Naturais e Sócio-Econômicos do Pantanal – Os vol. 3, no. 1, p. 110-129. desafios do novo milênio. Corumbá: Embrapa. p. 1-7. GUARIM-NETO, G. 1984. Plantas utilizadas na medicina popular SOUZA, LF. and GUARIM-NETO, G., 1999. Estudo etnobotânico cuiabana – um estudo preliminar. Revista da Universidade Federal em duas comunidades ribeirinhas: Coxipó do Ouro e São Gonçalo de Mato Grosso, vol. 4, no. 1, p. 45-50. – MT – Brasil. In Anais do II Simpósio sobre Recursos Naturais e Sócio-Econômicos do Pantanal. Corumbá: Embrapa. p. 471-478. GUARIM-NETO, G., 2006. O saber tradicional pantaneiro: as plantas medicinais e a educação ambiental. Revista Eletrônica do VERGER, PF., 1995. Ewê: o uso das planas medicinais na sociedade Mestrado em Educação Ambiental, v. 17, p. 71-89. Iorubá. São Paulo: Companhia das Letras. 762 p. HAMILTON, SK., SIPPEL SJ. and MELACK, JM., 1996. VIEGAS JUNIOR, C., REZENDE, A., SILVA, DHS., CASTRO- Inundation patterns in the Pantanal wetland of South America GAMBÔA, I. and BOLZANI, VS., 2006. Aspectos químicos, determined from passive microwave remote sensing. Archiv für biológicos e etnofarmacológicos do Gênero Cassia. Química Hydrobiologie, vol. 137, no. 1, p. 1-23. Nova, vol. 29, no. 6, p. 1279-1286. KUNWAR, RM., NEPAL, BK., KSHHETRI, HB., RAI, SK. and World Health Organization – WHO, 2002. WHO Traditional Medicine BUSSMANN, RW., 2006. Ethnomedicine in Himalaya: a case Strategy 2002-2005. Geneva: World Health Organization. 74 p.

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Coleoptera (Insecta) as forest fragmentation indicators in the Rio Negro sub-region of the Pantanal, Mato Grosso do Sul, Brazil Favero, S.*, Souza, HA. and Oliveira, AKM. Programa de Pós-graduação em Meio Ambiente e Desenvolvimento Regional, Universidade Anhanguera – Uniderp, Rua Ceará, 333, Bairro Miguel Couto, CP 2153,CEP 79003-010 Campo Grande, MS, Brazil *e-mail: [email protected] Received October 14, 2010 – Accepted December 13, 2010 – Distributed April 30, 2011

Abstract The purpose of this study was to evaluate the integrity of two forest fragments in Rio Negro Pantanal sub-region, using coleopterans as environmental indicators. The study was carried out at Santa Emilia Farm in the Rio Negro sub- region, municipality of Aquidauana, Mato Grosso do Sul (19o 30’ 18’’ S and 55° 36’ 45’’ W). Two sites were selected, locally denominated as “cordilheiras” (narrow and elongated strands of elevated soil), one with low degree of anthropic disturbance (CL) and the other, currently undergoing restoration process (TD). The sampling sites were determined using a GPS device. Ten pit-fall traps containing water and detergent were used for the specimens sampling, which were screened and identified. Abundance, richness, diversity and similarity were determined. Abundance was higher for CL (n = 277) than for TD (n = 251). The same was observed for the diversity indices, CL showed H’ = 2.83 bit.individual-1 and TD = 2.48 bit.individual-1, confirming the interferences made for abundance. Specimens of ten families were captured in CL area and seven families in TD area, indicating higher richness in CL, when compared to TD. The linear correlation coefficient (p > 0.05) indicates that both areas are significantly different, showing similarity value of 66.7%. The data show that the structure and disturbance degree in the environment integrity influence the composition of beetles fauna, causing the increase of abundance, richness and diversity in anthropogenic environments undergoing the early stage of regeneration. Keywords: biodiversity, flood plain, insects, coleopterans.

Coleoptera (Insecta) como indicadores de fragmentação florestal na sub-região do Pantanal do Negro, Mato Grosso do Sul, Brasil

Resumo Este trabalho avalia a integridade de dois fragmentos de floresta da sub-região do Rio Negro do Pantanal, utilizando coleópteros como indicadores. O estudo foi conduzido na Fazenda Santa Emília, na sub-região do Rio Negro, município de Aquidauana, Estado de Mato Grosso do Sul (19o 30’ 18’’ S e 55° 36’ 45’’ W). Dois estreitos fragmentos de floresta (localmente conhecida com cordilheira), situados em terrenos um pouco mais elevados, um com baixo grau de perturbação antrópica (CL) e o outro em processo de restauração (TD). Os sítios de amostragem foram marcados com GPS. Dez armadilhas de queda contendo água e detergente foram utilizadas. Abundância, riqueza de espécie, diversidade e similaridade foram determinadas. Abundância foi maior para CL (n = 277) do que para TD (n = 251). A mesma tendência foi observada para índices de diversidade, CL com 2,83 e TD com 2,48. Indivíduos de dez famílias foram capturados na área CL e de sete famílias na área TD, indicando mais alta riqueza em CL. O coeficiente de correlação linear (p > 0,05) indica que ambas as áreas são significantemente diferentes, com valor de similaridade de 66,7%. Os dados mostram que o grau de perturbação e estrutura da integridade ambiental influencia a composição da fauna de besouros, causando o aumento em abundância, riqueza e diversidade nos dois fragmentos estudados. Palavras-chave: biodiversidade, planície de inundação, insetos, coleópteros.

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1. Introduction developed for the utilisation in pollution control in rivers and lakes. It is based on the use of species present in the A forest fragment can be defined as “any area of community and subjected to some kind of evolutionary continuous natural vegetation, interrupted by anthropic impact, in the past, or anthropogenic impact in the present barriers (roads, agricultural crops, etc.), or natural ones (Correia, 2002). (lakes, other vegetation types, etc), capable of significantly Due to its biological importance, entomofauna is reducing the flow of animals, pollen, and/or seeds” normally used as an evaluation parameter of fragmented (Tabanez et al., 1997). The structure and dynamic of areas. This group is one of the most important, because they forest fragments vary depending on several factors, mainly comprise about 59% of all existing animals (759,000 species the history of disturbance, the area’s shape, the type of formally described), however they have been rarely used neighbouring environments and the isolation degree and, as “flagship species” in the conservation of natural areas. depending on these characteristics, can be self-sustaining Although birds and mammals are most appreciated by or not (Tabanez et al., 1997). conservationists in general, the usefulness of insects as Struminski and Lorenzotto (2003) emphasises the environmental indicators is unquestionable. Some groups, obvious importance of knowledge about fragmentation among which butterflies, beetles and ants, are especially nowadays, because in many landscapes vast numbers of useful in environmental monitoring since they are easily species are restricted to fragments. In the State of Mato sampled and identified, found all year round, and show Grosso do Sul, there is a typical ecosystem, popularly known as “Pantanal”, with landscapes formed by complex fast response to environmental changes. Therefore, they of natural environments or habitats that comprise a set can provide more information than vertebrates in general, of natural forest fragments interspersed among ponds due to their great usefulness in characterising small (“baías”), drainage channels (“vazantes” and “corixos”) fragmented areas or with a long history of anthropogenic and rivers, forming a landscape mosaic. influence habitats, where many of the most sensitive and In this region there are different vegetation physiognomies large vertebrates have already been eliminated by the such as areas with riparian and gallery forests, savannas reduction in living and hunting areas (Freitas et al., 2003). (forested, wooded and open grassland sub-types) which Insect diversity influences ecosystem dynamics through have several regional denominations such as “capões”, numerous mechanisms such as litter decomposition, “cordilheiras”, “cambarazais”, “paratudais”, among others. pollination, growth suppression of plants or serving as Normally, these phytophysiognomies are not extensive, prey to carnivores. According to their role in ecosystem being interspersed with other landscape types. The gradient dynamics, these invertebrates are classified in three of forested, wooded, shrub and grassland formations is categories: explorers, acting as herbivores, parasitoids or determined by topography, edaphic factors and mainly predators; suppliers, serving as hosts to parasitoids or preys seasonal conditions like the dry and wet periods, because to predators; and facilitators, acting as pollinators, pathogen annual flooding, when more than 50% of the region is vectors or phoresy (Thomazini and Thomazini, 2000). covered by water, contributes significantly to the formation Regarding the choice of key insect groups for studies of these environments (Magalhães, 1992). in fragmented forest systems, the most important ones The understanding of the biological dynamics of these are those capable of inducing physical changes in their habitats contributes to the comprehension of the Pantanal environment and regulate the availability of resources to biome as a whole, allowing a diagnosis of the behaviour other species, such as pollinators, seed predators, parasitoids of certain species in existing forest fragments. One of the and decomposers (Didham et al., 1996). more accessible groups to this type of study, already used Among these groups, the beetles of the family as environmental quality indicators, is that of entomofauna Scarabaeidae (Coleoptera) are used as indicators in (Freitas et al., 2003). studies on diversity of insects or arthropods and considered Alho (2003) describes indicators as signs or evidences essential in studies on forest fragmentation, since much of that enable researchers to verify the amplitude of variations the food (feces and carcasses) of this group is produced which the observed phenomenon is suffering, due to specific by organisms strongly affected by this process, such as processes or interventions. Therefore, various types of birds, primates and other large mammals (Lovejoy et al., indicators can be established: context indicators – when 1986). Furthermore, they are important in soil nutrients is desired to monitor events or situations related to a wide recycling, in the control of parasites of some vertebrates region; process indicators - when what becomes important and in seed dispersal (Klein, 1989). The utilization of these is the observation of the actions sequence or behaviour beetles as indicators in biodiversity survey programmes interactions, in a time scale; impact indicators - when the has also been suggested, owing to the great morphological, purpose is to check the effects pertinent to general goals, taxonomic, ecological and behavioural variability, sensitivity such as the number of species in an area designated for to environmental changes and abundance (Thomazini and monitoring. Thomazini, 2000). The use of indicator species to assess and monitor Accordingly, this study aims to evaluate the integrity biological processes in the ecosystems dates from the of forest fragments in the Rio Negro Pantanal sub-region, early twentieth century. Later this concept was largely using Coleoptera species as environmental indicators.

292 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 291-295 Coleoptera as forest fragmentation indicator in the Pantanal

2. Material and Methods The sampled specimens were stored in glass bottles properly covered and containing ethylic alcohol (70%), The study was conducted at Santa Emilia Farm (Rio which were labelled (date, sampling place and time) and Negro Pantanal’s sub-region), municipality of Aquidauana, transported to the Entomology Lab of Anhanguera-Uniderp Mato Grosso do Sul, 270 km from Campo Grande, University for screening, taxonomic identification and, where the Instituto de Pesquisa do Pantanal – IPPAN, then, deposited in the scientific collection. Statistical of Universidade para o Desenvolvimento do Estado e da treatment was performed to determine the abundance, Região do Pantanal – UNIDERP, is situated. In this area richness (jackknife1), diversity (Shannon index, log 10), there is a diversity of environmental conditions, with a large similarity (SØrensen) and evenness of the species occurring variety of vegetation types including riparian and gallery in the sampling sites (Krebs, 1989). forests, which occupy large areas along the “Correntoso River”, and the typical forests of “cordilheiras”, narrow 3. Results and Discussion and elongated strands of elevated soil (1-2 m) above floodable grasslands. It has been suggested that they are 3.1. Abundance and diversity ancient dunes covered by “cerradão” vegetation (forested savanna), presenting tall trees (12-16 m) and shorter ones In this study, 528 coleopterans distributed in 10 families (3-7 m) (Alho and Gonçalves, 2005). were collected. The largest number of specimens (277) The woody vegetation of this formation, with its sandy was captured in the area denominated “Cordilheira do soil, has typical species, with emphasis on the occurrence Lau” (CL), and the lowest number in “Cordilheira das of “Cambará” (Volchysia divergens, Pohl), “Tarumã” (Vitex Três Divisas” (TD) (251) (Table 1). cymosa Bertero), “Jatobá mirim” (Hymenaea sp. L.), Abundance was higher in CL, which demonstrates the “Ximbuva” (Enterolobium sp. Mart.), “Novateiro” (Triplaris advanced restoration degree of the vegetation compared to the TD area. The greater abundance in the CL area is due americana L.), “Paratudo” (Tabebuia aurea (Manso)), to the higher number of species of the family Scarabaeidae “Manduvi” (Sterculia apetala (Jacq)), “Piuva” (Tabebuia (13) collected during the four samplings and also to the sp. Gomes ex D.C.), “Gonçalo” (Astronium fraxinifolium significant occurrence of the species 5 of Scarabaeidae Scott), “Embaúba” (Cecropia pachystachya Trec.), “Acuri” (134) in the first sampling in CL area (Table 1). These (Attalea phalerata Mart.), “Figueiras” (Ficus sp. L.), insects help in dispersal and burial of seeds, with potential “Pequi” (Caryocar brasiliense L.), ”Bocaiúva” (Acrocomia long-term effects on forest maintenance or restoration aculeata Jacq.), “Lixeira” (Curatella americana L.), (Lewinsohn et al., 2005). Similar results were obtained “Cumbaru” (Dipteryx alata Vog.), “Maminha-de-porca” by Marinoni and Ganho (2003, 2006) and Ganho and (Zanthoxylum rigidum Humb). In the shrub stratum, the Marinoni (2003) in anthropogenic areas of Araucaria in presence of representatives of the families Rubiaceae the state of Paraná. and Myrtacea was registered, among others (Pott and These numbers may be associated with the greater Pott, 2003). In the vicinity of the “cordilheira”, natural diversity of feeding habits of the coleopterans and to the grasslands are encountered constituted by “capim barba-de- greater availability of floristic resources in regeneration velho” ( virgatum D.C.) and “capim navalha” areas. The elevated number of individuals of certain plant (Scleria melaleuca Rchb. ex Schltdl. & Cham.), where species leads to large production of fruits, that attract scattered clumps of “Canjiqueiras” (Birsonima sp Rich specific coleopterans and mammals that feed on them, ex Kunth.) are found. leaving in place large amount of feces, which also attract For the field work execution and data sampling, two other organisms. Hutcheson (1990) mentions that in more sites with low anthropogenic influence and 3,096.42 m open habitats at the climax stage and dominated by shrubs, apart from each other were previously established. In the fewer individuals were captured comparing to restoration past, selective extractions of wood were undertaken in areas, in the same ecosystem type. these locations, but are currently undergoing advanced This feature can also be observed when comparing the regeneration process. diversity indices calculated for each studied area, CL showed The first site is located near the region locally known as H’= 2.83 bit. individuals-1 and TD H’= 2.48 bit.indivíduo-1, “baía do cervo”, which is bordered by a “cordilheira” that confirming the inferences made for abundance (Table 2). received the denomination “Cordilheira das Três Divisas” (TD), located at 19° 30’ 23’’ S and 55° 35’ 32’’ W. 3.2. Family richness The second site is located near the Santa Marta Farm Ten families were found in the CL area and seven boundary, in a “cordilheira” that received the denomination families in TD, consequently CL showed greater family “Cordilheira do Lau” (CL), located at 19° 29’’ 24’’ S and richness (Tables 1 and 2). 55° 36’ 38’’ W. Regarding the Brazilian coleopterofauna, Costa Lima The sampling effort was undertaken through the (1952) listed 112 families, Costa et al. (1988) listed installation of 10 pit-fall traps, containing water and 109 families, and Costa (1999) 106 families. This variation detergent, and the captured insects were collected at is an outcome of constant revisions of the coleopterans dawn (Almeida et al., 1998). Four sampling sessions classification. In the present work, the low family richness were performed. found is probably due to the sampling method, since the

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 291-295 293 Favero, S., Souza, HA. and Oliveira, AKM. attractants, baits or lures were not used in the traps, which the native mammalian fauna (feral pigs, capybaras, tapirs, were randomly installed in the studied areas. primates) and birds. Agropastoral activity within and in the The greatest richness in CL can be explained by the surrounding area also serves as a resource for necrophagus highest productivity of this area, that displays regeneration and coprophagus species, which feed on these ruminants degree with higher regrowth, flowering and leaves and fruits feces as explained by Thomazini and Thomazini (2000). falling, that provide resources for phytophagous species, Therefore, it is possible to observe that the difference besides the presence of feces and carcasses resulting from between the areas may be conditioned by the presence of rare individuals and not by the degree of preservation, as affirmed by Ganho and Marinoni (2003). Table 1. Families of Coleoptera collected in two 3.3. Community structure “cordilheiras” of Rio Negro Pantanal sub-region, Santa Emília Farm, Mato Grosso do Sul. Similarity 1 1 Taxon Morphotype TD CL The structures of coleopteran communities in the Bruchidae 1 0 1 TD and CL areas, based on the total values of species Carabidae 1 9 4 abundance, are not significantly similar (linear correlation 2 63 44 coefficient p > 0.05) (Table 2). 3 1 2 Both sampling areas demonstrate independent community structure, showing 66.7% similarity, due to the approximate 4 1 1 number of species richness in each area, associated to the 5 0 1 proportionally low number of shared species (17 species 6 2 1 of the 54 registered) (Table 1). Considering that the 7 0 4 physiognomic characteristics of the areas are different, 8 1 1 and considering their floristic diversity, the similarity Cerambycidae 1 0 1 value of coleopterans species between the areas is low. Marinoni and Ganho (2003, 2006); Ganho and Marinoni Chrysomelidae 1 3 3 (2003) researched areas of Araucaria forest in the state of 2 2 2 Paraná, and found greater similarity between the different 3 1 1 studied areas, however the dominance of a single plant 4 0 1 species, the araucaria, favours the similarity between insect Curculionidae 1 18 11 species since the floristic richness is the same. 2 9 3 3 1 0 4. Conclusions Histeridae 1 1 1 The abundance and diversity of insects in the “CL”, an Nitidulidae 1 0 2 area undergoing more advanced stage of floristic restoration, 2 1 3 are higher than the “TD”, undergoing initial stage of Staphilinidae 1 0 3 restoration. The same pattern was verified for family richness, indicating higher values for the “CL” site compared to the Scarabaeidae 1 118 33 “TD” site, in less advanced stage of restoration. There is 2 1 1 3 11 9 4 5 2 Table 2. Estimated and maximum richness, estimated and 5 0 134 maximum diversity, evenness and similarity between the 6 0 1 two “cordilheiras” in the Rio Negro Pantanal sub-region, 7 0 1 Santa Emília Farm, Mato Grosso do Sul, 2005. 8 0 1 Fragment Parameter 9 0 1 CL1 TD 10 0 1 Abundance 277 251 11 0 1 Richness (Jackknife) 33 21 12 1 1 Maximum richness (Jackknife) 49.5 21 13 1 0 Diversity (Shannon) 1.9628 1.7166 Tenebrionidae 1 1 0 Maximum diversity (Shannon) 3.4965 3.0445 2 0 1 Evenness 0.5613 0.5638 Total -x- 251 277 Similarity 0.667 r = 0.288 ns 1/TD = “Cordilheira das Três Divisas”; CL = “Cordilheira CL = “Cordilheira do Lau”; TD = “Cordilheira das Três do Lau”. Divisas”; 1/ns = non significant (p > 0.05).

294 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 291-295 Coleoptera as forest fragmentation indicator in the Pantanal significant difference in the coleopterofauna composition Abundância e Riqueza das famílias capturadas através de armadilhas between the areas, showing a low coefficient of similarity. malaise. Revista Brasileira de Zoologia, vol. 24, no. 4, p. 727-736. Therefore, the structure and the disturbance degree of HUTCHESON, J., 1990. Characterization of terrestrial insect the environments integrity influence coleopterofauna communities using quantified, Malaise-trapped Coleoptera. composition, causing the increase of abundance, richness Ecological Entomology, vol. 15, p. 143-151. and diversity in anthropogenic environments and those KLEIN, BC., 1989. Effects of forest fragmentation on dung undergoing advanced stage of restoration. and carrion beetle communities in Central Amazonia. Ecology, vol. 70, no. 6, p. 1715-1725. References KREBS, CJ., 1989. Ecological methodology. New York: Harper‑Collins. 654 p. ALHO, CJR., 2003. Conservação da biodiversidade da Bacia do Alto Paraguai. Campo Grande: Editora Uniderp, 2003. 466 p. LEWINSOHN, TM., FREITAS, AVL. and PRADO, PI., 2005. Conservação de invertebrados terrestres e seus habitats no Brasil. ALHO, CJR. and GONÇALVES, HC., 2005. Biodiversidade do Megadiversidade, vol. 1, no. 1. Pantanal: ecologia & conservação. Campo Grande: Ed.Uniderp. 142 p. LOVEJOY, TE., BIRREGAARD JUNIOR, RO. and RYLANDS, AB., 1986. Edge and other effects of isolation on Amazon forest ALMEIDA, LM., RIBEIRO-COSTA, CS. and MARINONI, L., fragments. In SOULÈ, ME., ed. Conservation biology: the science of 1998. Manual de coleta, conservação, montagem e identificação scarcity and diversity. Sunderland: Sinauer Associates. p. 257-285. de insetos. Ribeirão Preto: Holos. 78 p. MAGALHÃES, NW., 1992. Conheça o Pantanal. São Paulo: CORREIA, MEF., 2002. Potencial de Utilização dos Atributos Terragraph. p. 390. das Comunidades de Fauna de Solo e de Grupos Chave de Invertebrados como Bioindicadores do Manejo de Ecossistemas. MARINONI, RC. and GANHO, NG., 2003. Fauna da Coleoptera Seropédica: Embrapa Agrobiologia. 23 p. Embrapa Agrobiologia, no Parque Estadual de Vila Velha, Ponta Grossa, Paraná, Brasil. Documentos, no. 157. Abundância e Riqueza das famílias capturadas através de armadilhas COSTA, C., 1999. Coleoptera linnaeus, 1758. In: JOLY, CA. de solo. Revista Brasileira de Zoologia, vol. 24, no. 4, p. 727-744. and BICUDO, C., Org. Biodiversidade do Estado de São Paulo. -, 2006. A diversidade diferencial beta de Coleoptera (Insecta) em Síntese do conhecimento ao final do século XX. São Paulo: uma paisagem antropizada do Bioma Araucária. Revista Brasileira FAPESP. p. 115-122. de Entomologia, vol. 50, no. 1, p. 64-71. 2006. COSTA, C., VANIN, SA and CASARI-CHEN, SA., 1988. POTT, A. and POTT, V., 2003. Espécies de fragmentos florestais Larvas de Coleoptera do Brasil. São Paulo: Museu de Zoologia, em Mato Grosso do Sul. In COSTA, RB. Fragmentação florestal Universidade de São Paulo. 282 p. e alternativas de desenvolvimento rural na região Centro-Oeste. COSTA LIMA, AM., 1952. Coleópteros. In: Costa Lima, AM. Campo Grande: UCDB. p. 26-52. Insetos do Brasil. Rio de Janeiro: Escola Nacional de Agronomia. STRUMINSKI, E. and LORENZETTO, A., 2003. A fragmentação vol. 7. 372 p. de ecossistemas na Área de Proteção Ambiental – APA do Rio DIDHAM, RK., GHAZOUL, J., STORK, NE. and DAVIS, AJ., Passaúna – Região Metropolitana de Curitiba – PR. Cadernos da 1996. Insects in fragmented forests: a functional approach. Tree, Biodiversidade/Diretório de Biodiversidade e Áreas Protegidas, vol. 11, no. 6, p. 255-260. vol. 4, no. 1. FREITAS, AVL., FRANCINI, RB. and BROWN Jr., K., 2003. TABANEZ, AJ., VIANA, VM. and DIAS, AS.,1997. Conseqüências Insetos como indicadores ambientais. In CULLEN Jr., L., da fragmentação e do efeito de borda sobre a estrutura, diversidade RUDRAN, R. and VALLADARES-PADUA, C. Métodos de e sustentabilidade de um fragmento de floresta de planalto de estudos em biologia da conservação & manejo da vida silvestre. Piracicaba, SP. Revista Brasileira de Biologia = Brazilian Journal Curitiba: Ed. da UFPR; Fundação O Boticário de Proteção à of Biology. vol. 57, no. 1, p. 47-60. Natureza. p. 125-151. THOMAZINI, MJ. and THOMAZINI, APBW., 2000. A fragmentação GANHO, NG. and MARINONI, RC., 2003. Fauna da Coleoptera florestal e a diversidade de insetos nas florestas tropicais úmidas. no Parque Estadual de Vila Velha, Ponta Grossa, Paraná, Brasil. Rio Branco: Embrapa Acre. 21 p. Documentos, no. 57.

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Terrestrial and aquatic mammals of the Pantanal Alho, CJR.a*, Camargo, G.b* and Fischer, E.c* aPrograma de Pós-graduação em Ambiente e Desenvolvimento Regional, Universidade Anhanguera – Uniderp, CEP 79037-280, Campo Grande, MS, Brazil bPrograma de Pós-graduação em Ecologia e Conservação, Universidade Federal de Mato Grosso do Sul – UFMS, CEP 79070-900, Campo Grande, MS, Brazil cDepartamento de Biologia, Universidade Federal de Mato Grosso do Sul – UFMS CEP 79070-900, Campo Grande, MS, Brazil *e-mail: [email protected], [email protected], [email protected] Received October 14, 2010 – Accepted December 13, 2010 – Distributed April 30, 2011 (With 1 figure)

Abstract Different works have registered the number of mammal species within the natural habitats of the Pantanal based on currently known records, with species richness ranging from 89 to 152 of annotated occurrences. Our present list sums 174 species. However, at least three factors have to be emphasised to deal with recorded numbers: 1) to establish the ecotone limit between the floodplain (which is the Pantanal) and its neighbouring domain like the Cerrado, besides the existence of maps recently produced; 2) the lack of intensive surveys, especially on small mammals, rodents and marsupials; and 3) the constant taxonomic revision on bats, rodents and marsupials. Some species are very abundant - for example the capybara Hydrochoerus hydrochaeris and the crab-eating fox Cerdocyon thous, and some are rare, and others are still intrinsically rare - for example, the bush dog Speothos venaticus. Abundance of species is assumed to reflect ecological resources of the habitat. Local diversity and number of individuals of wild rodents and marsupials also rely on the offering of ecological resources and behavioural specialisation to microhabitat components. A large number of species interact with the type of the vegetation of the habitat, by means of habitat selection through active patterns of ecological behaviour, resulting on dependency on arboreal and forested habitats of the Pantanal. In addition, mammals respond to seasonal shrinking-and-expansion of habitats due to flooding regime of the Pantanal. The highest number of species is observed during the dry season, when there is a considerable expansion of terrestrial habitats, mainly seasonally flooded grassland. Major threats to mammal species are the loss and alteration of habitats due to human intervention, mainly deforestation, unsustainable agricultural and cattle-ranching practices, which convert the natural vegetation into pastures. The Pantanal still harbours about a dozen of species officially listened as in danger. Keywords: biodiversity, conservation, Pantanal habitats, mammal species, environmental threat.

Mamíferos terrestres e aquáticos do Pantanal

Resumo Diversos trabalhos têm registrado o número de espécies de mamíferos nos diferentes hábitats naturais do Pantanal, com base nos registros do conhecimento corrente, com a riqueza de espécies variando de 89 a 152 ocorrências anotadas. Nossa lista atual soma 174 espécies. Contudo pelo menos três fatores devem ser enfatizados quando se lida com os números encontrados: 1) o limite exato do ecótono entre a bacia de inundação (que é o Pantanal) e os domínios vizinhos, como o Cerrado, apesar da existência de mapas recentes; 2) a falta de levantamentos intensivos, particularmente sobre pequenos mamíferos, roedores e marsupiais; e 3) a revisão taxonômica constante de morcegos, roedores e marsupiais. Algumas espécies são abundantes, como a capivara Hydrochoerus hydrochaeris, e o lobinho Cerdocyon thous, outras são raras e outras ainda são intrinsecamente raras, como o cachorro-vinagre Speothos venaticus. Assume-se que a abundância de espécies reflete os recursos ecológicos contidos nos hábitats. A diversidade local e o número de indivíduos de roedores silvestres e marsupiais também dependem da oferta ecológica de recursos e da especialização de comportamento para explorar componentes de micro-hábitats. Grande número de espécies interage com os tipos de vegetação do hábitat, por meio de seleção de hábitat com padrões ativos de comportamento ecológico, que resultam na dependência dos mamíferos de hábitats arbóreos e florestados do Pantanal. Além disso, os mamíferos respondem ao encolhimento e expansão dos hábitats devido à inundação sazonal do Pantanal, com abundância de espécies mais altas na estação seca, quando há considerável expansão de hábitats terrestres, principalmente campos inundáveis. As ameaças mais importantes para os mamíferos são a perda e alteração de hábitats devido à intervenção humana, particularmente o desmatamento, práticas de agricultura e pecuária insustentáveis, com conversão da vegetação natural em pastos. O Pantanal ainda abriga cerca de uma dúzia de espécies oficialmente ameaçadas de extinção. Palavras-chave: biodiversidade, conservação, hábitats do Pantanal, espécies de mamíferos, ameaças ambientais.

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 297-310 297 Alho, CJR., Camargo, G. and Fischer, E.

1. Introduction habitat requirements, to understand mammalian dynamics. Our study also identifies major environmental threats The Pantanal wetland is largely known worldwide dealing with a conservation agenda. Joining the available for its extraordinary wildlife, particularly the mammal information, we approach comprehensive patterns of species, which include jaguar, capybara, marsh deer, mammalian ecology, combining habitat features and species giant anteater, and many others, interacting in complex interactions in search of unifying trends for the species, ecological communities. The Pantanal is composed of different landscapes constituted of habitat gradients populations and communities to the drastically seasonal which offer feeding and reproductive ecological niches, habitats. The relevant literature on species occurrence, sustaining a high diversity of mammal species. The high community composition, population densities, habitat heterogeneity of the Pantanal promotes the selection of preference, and interspecific relations of mammals in the different habitats by species which widely overlap in habitat Pantanal was surveyed. use. The Pantanal community compositions are subject The reviewing of records of Pantanal mammals was to an annual hydrological cycle which determines the based on previous revisions and additional scientific literature ecosystem functioning and the high seasonal productivity, and technical reports (Marinho-Filho and Sazima, 1998; supporting a diverse and abundant fauna, including large Wilig et al., 2000; Oliveira et al., 2002; Rodrigues et al., and endangered mammal species (Alho et al., 1988; Alho, 2002; Camargo and Fischer, 2005; Longo et al., 2007; 2005a, 2008). These factors have influenced diversity Marinho-Filho, 2007; Carmignotto, 2004; Cáceres et al., throughout life history and nowadays also influence the 2008; Aragona and Marinho-Filho, 2009; Tomás et al., presence of species competing for daily needs to survive 2010). Species names follow Wilson and Reeder (2005) and reproduce. and Reis et al. (2006); classes of extinction threats follow Several surveys on a different time scale have shown the International Union for Conservation of Nature (IUCN) the great magnitude of the mammalian fauna of the and the Livro Vermelho da Fauna Brasileira Ameaçada de Pantanal: on mammalian biomass (Schaller, 1983), on Extinção (IBAMA) of the Ministério do Meio Ambiente occurrence of species (Alho et al., 1988; Trolle, 2003), of (Brazilian Ministry of the Environment). a literature review (Coutinho et al., 1997; Rodrigues et al., 2002), on working group results (Marinho Filho, 2007), 3. Results and Discussion on responses to seasonal flooding (Mamede and Alho, 2006), on microhabitat use among small mammals (Lacher 3.1. Richness of Pantanal mammals and Alho, 1989), on ecology (Alho, 2005a, 2008), and studies on single species such as capybaras (Alho et al., The total number of mammal species that occur in 1989; Alho, 2003), jaguar (Soisalo and Cavalcanti, 2006; the Pantanal wetland has been previously reported to Azevedo and Murray, 2007), march deer (Schaller and vary between 89 and 152 (Alho et al., 2003; Alho, 2005a; Vasconcelos, 1978; Mauro et al., 1998; Mourão et al., Cáceres et al., 2008; Coutinho et al., 1997; Marinho Filho, 2000), ocelot (Trolle and Kéry, 2005), and other studies. 2007; Reis et al., 2006; Sabino and Prado, 2006; Tomás et al., Pantanal land use is altering natural habitats to 2010). According to the working group designated by the accommodate human needs. The landscape has been Ministry of Environment (Ministério do Meio Ambiente; modified by human intervention, mainly deforestation, see Marinho Filho, 2007) there are officially 132 species unsustainable agricultural and cattle-ranching practices, of mammals in the Brazilian Pantanal. Here we update this which convert the natural vegetation into pastures (Alho et al., number to 170 mammal species in the Brazilian Pantanal, 1988; Alho, 2005a, 2008; Harris et al., 2005). Therefore, and to 174 species including the Pantanal floodplain in some natural habitats are in distress. The aim of this review Northeastern Paraguay (Willig et al., 2000). The increased is to present comprehensive ecological information that number of species reviewed here is partially related to forms the magnitude foundation of the mammal species constant progress in taxonomic revisions, especially diversity in the Pantanal. We check out the mammal species with the support of cytogenetics to identify new species already reported to occur in the Pantanal, and discuss the of small mammals (wild rodents and marsupials), and to relevant patterns of habitat use and conservation strategies. the recently increase of surveys on bats – by far the richer Secondarily, the purpose here is to identify new lines order of mammals in the Pantanal (Figure 1) (Camargo of research (new perspectives, initiatives, analyses and and Fischer, 2005; Longo et al., 2007; Santos et al., 2010). interpretations) to motivate work to elucidate complex Despite several mammal species being conspicuous in the ecological phenomena, through environmental parameters, Pantanal, like capybara – a symbol of the Pantanal – most instead of simple lists of species occurrence. of the mammal species are not easily recorded, as they present nocturnal and twilight habits. Thus, an increase 2. Methods in the number of mammal species is also expected as a We synthesise the literature in order to update recent result of improved sampling methods. Although additional developments on occurrence of wild mammal species in the species have been found over time, another difficulty to Pantanal , as well as firmly relying on our two-decade work set the right number of mammal species is the problem experience in the region, to identify diversity, abundance, in determining the exact limits of the Pantanal floodplain

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Figure 1. Species richness of nine orders of mammals which occur in the Pantanal floodplain.

relative to the surrounding domains of Cerrado, Amazonia, Species abundance is often assumed to be the result of and Chaco. availability of resources, for example, preferable habitats The Pantanal is a savanna wetland (Alho, 2005a) and with a large offering of feeding and reproductive niches. This its biota is closer to that of Cerrado (195 mammal species), is the case of resources that affect the number of mammal with some Amazonian and Chaco biogeographic influences. species with a wide range of zoogeographical distribution The flatland (80-150 m in altitude) has been considered the like the capybara, marsh deer, crab-eating fox, but it does floodplain (Pantanal), and its surrounding Cerrado upland not apply to some species which are rare throughout all plateaus (200-1,200 m in altitude) is known as planalto. their distribution range, including the Pantanal, as is the It helps to establish the Pantanal limits to some extent, case of the bush dog, which seems to be attached to greater but difficulties remain due to the complex maze of mosaic ecological and behavioural specialisation, the strategy of habitats, under different seasonal flooding regimes (Alho, which is to be intrinsically rare. 2008). There are official maps delimiting these bounders in The patterns of habitat intergradations are even more the Paraguay river basin (ANA, 2004) as well as tentative complex in ecotone zones of broad contact between the delimitations of the Pantanal and its subregions based on Pantanal and Cerrado (Lacher and Alho, 2001). Habitat is criteria of flooding, relief, soil and vegetation type (Silva an important factor in mammalian community structure. and Abdon, 1998). However, for mobile animals like wild Vegetation types in different habitats influence mammal mammals, these limits are unreasonable. Additionally, species. The physiognomic units of the Pantanal are human activities have modified the landscape and so wild characterised by their phytosociological and ecological mammal occurrence and local distribution are changing arrangements, forming well-defined landscape units like (Alho, 2008). Unprecedented mammal species have seasonal flooding open fields, arboreal patches of savanna been recorded in the uplands surrounding the Pantanal or capões de cerrado, semi-deciduous forest on upper (e.g. Alho, 2000), and part of them might be expected to grounds or cordilheiras, riverine and gallery forests, additionally occur in the floodplain. and others (Alho, 2005a; Silva et al., 1998). Therefore, the offering of different resources, particularly food and 3.2. Habitats and resources niches for reproduction, influences social systems of most The observed abundance of some species in the Pantanal populations of Pantanal mammals and determines local habitats reveals that only a few species are common – for species richness, abundance, and competition. example the capybara Hydrochoerus hydrochaeris, the Abundance of capybaras in the Pantanal varies seasonally, crab‑eating fox Cerdocyon thous, and the flat-faced affected by changes in food abundance and available space fruit‑eating bat Artibeus planirostris – whereas some due to annual flooding (Alho et al., 1989). Capybara’s group are rare or intrinsically rare – for example, the bush dog sizes increases from the end of the rainy season to the dry Speothos venaticus (Alho et al., 1988, 1989; Mamede and season, when there are more young in the groups. During Alho, 2006; Alho, 2005a, 2008; Teixeira et al., 2009). the dry season more capybaras are observed feeding on the

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 297-310 299 Alho, CJR., Camargo, G. and Fischer, E. pasture of the seasonal flooding open fields. In fact, higher woodland-dwelling genera such as Cerradomys and densities of other mammal species occur during the dry Oligoryzomys occur within a few metres of transition season (August and September), when there is a considerable zone-habitat dwellers such as Clyomys and Trichomys. expansion of terrestrial habitats, mainly seasonally flooded The genus Oligoryzomys also occur in both open and grassland, due to the shrinking-and‑expansion of habitats forested habitats. related to the flooding pulse (Mamede and Alho, 2006). Microhabitat use among small mammals in the Pantanal Capybara Hydrochoerus hydrochaeris and caiman shows that two genera of Cicretidae rodents – Oligoryzomys Caiman yacare are the most common wild species killed (with two species occurring in the Pantanal: O. chacoensis by jaguars Panthera onca in the Pantanal (Azevedo and and O. microtis) and Cerradomys (C. subflavus) –are Murray, 2007), and both prey species are equally abundant more generalised in their use of microhabitats than are in the region. Jaguars also consume a high variety of prey, two Echimyidae species - Clyomys laticeps and Trichomys including deer, peccary and others. It was estimated that pachyurus (referred to as T. apereoides in some publications, the wild prey base was adequate to support the jaguar but recognised as a distinct species based on chromosomal population in the study area. The study also concluded differentiation; Bonvicino and Lacher, 2008). Oligoryzomys that spacing patterns in the local jaguar population were species are broad habitat generalist at the “Nhecolândia” likely based on exclusion through territoriality rather than sub-re­gion of the Pantanal. Cerradomys subflavus patches food limitation. of arboreal savanna, capão de cerrado. Both Clyomys and The total home range size area of five females and Trichomys were restricted to their transition microhabitat. three male jaguars in the study area was 112.2 km² (density Although both genera overlap in the same microhabitat, of 0.07 adult resident jaguars per square kilometre). competition is avoided since Trichomys is scansorial while Home‑range size was comparable between sexes; almost Clyomys is fossorial (Lacher and Alho, 1989). In general half of their home range areas was shared with conspecifics the transition between arboreal habitats and open areas are of the same sex, but little overlapping was observed at the selected by Trichomys pachyurus (Carmignotto, 2004). core areas, suggesting that same-sex resident individuals Studies carried out in habitats surrounding the Pantanal, established exclusive core areas (Azevedo and Murray, on plateaus of Chapada dos Guimaraães, state of Mato 2007). These results indicate that prey abundance was Grosso, pointed out that the combination of vegetation type sufficiently abundant to influence patterns of exclusivity in and substrate structured the community of 19 terrestrial the spatial distribution of resident jaguars and hence prey species of small mammal into several smaller communities selection patterns. Although there is indication that prey with little faunal overlap (Lacher and Alho, 2001). This availability influences jaguar populations in the Pantanal, study showed that most species were captured in only one spatial patterns seem to be influenced by a territorial or two of the qualitative habitat types. There were open system, governed by regions of exclusivity (home range habitat species completely absent from forest, and forest and territory), rather than by prey abundance (Azevedo species that were captured only in forest habitats. Cluster and Murray, 2007). analysis of 19 species studied confirmed the separation made by qualitative classification of habitats based on plant 3.3. Microhabitats and ecological resources species composition and other habitat characteristics. The Local diversity and number of individuals also rely on results for habitat associations of small mammal species the offering of resources and behavioural specialisation to determined by cluster analysis of soil and vegetation habitat components. On a small scale, specialised species structural characteristics (independently of plant species are able to exploit the spatial and temporal variation of the composition) generated five fairly distinct clusters. habitat heterogeneity, including microhabitat components The gallery forest cluster grouped the same set of (Lacher and Alho, 1989; Alho, 2005b; Carmignotto and species that had previously been assigned to gallery forest Monfort, 2006). In the Cerrado landscape, small mammal (Neacomys spinosus, Hylaeamys megacephalus, Nectomys communities differ along a gradient of natural habitats squamipes, Oecomys bicolor, Proechimys longicaudatus, (Alho, 2005b). Community differences appear to be a and Caluromys philander), confirming the earlier analysis. function of local mosaic factors as well as differences The cluster analysis also grouped the six species that had among river basins, between high plateau forested habitats previously been associated with wet field (Oligoryzomys and lowland valley forests, or between moister open areas microtis — occurring at the Cerrado-Amazonia contact with soft soil and abundant grass versus very dry and zone, Oligoryzomys nigripes (= eliurus), Cerradomys rocky microhabitats. For example, among small mammals, subflavusspecies group, Necromys lasiurus, Monodelphis like marsupials and rodents, there are habitat generalists domestica, and Marmosa murina). The grouping of occurring in more than three types of habitat (pan-habitat species was essentially the same whether it was done species) and habitat specialists, showing a high degree of qualitatively by habitat type or by a quantitative analysis fidelity to habitat. of structural aspects of the vegetation and substrate of It is common to find small mammal species with a the habitat (Lacher and Alho, 2001). Small mammals are preference for arboreal or forested habitats or for open more specialised regarding to habitat requirements, and habitats within the same study area. In the semi-decidous so they are able to exploit different parts of the habitat forest habitats, surrounded by open savanna habitats, mosaics of the Pantanal.

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3.4. The dependence of forest habitats strata, occupied by mammal species. In general the fauna The Pantanal habitats support a number of living of the Pantanal and the surrounding Cerrado present mammal species that interact with each other and with the strong dependency on habitat complexity (Alho et al., type of the vegetation of the habitats. How these mammal 2003; Alho, 2008). species interact with the type of the vegetation is a result of Analyses using the 15 most abundant mammal species in habitat selection by means of active patterns of ecological the Pantanal habitats (considering macroniche characteristics) behaviour. This interaction will then determine how a have pointed out that at least ten mammal species strongly rely given species well uses the range of habitats to fulfill its on the presence of arboreal or forested habitats (Alho et al., daily need for food, space, shelter, social interactions, 2003). This dependence on arboreal/forest habitats can reproduction and other living requirements, as a result be evaluated as a function of the characteristics of the of habitat selection. The local presence of these required macroniche used by each mammal species, considering habitat needs, like forest areas, are essential to determine the body size, its requirement of habitat quality, and its population and community parameters like species richness, type of diet and locomotion. Five species (Alouatta caraya, abundance, reproductive potential and other. Nasua nasua, Dasyprocta punctata, Cerdocyon thous and In the Pantanal there are different mammal species that Mazama americana) are dependent on arboreal/forest rely on forest or arboreal habitats, besides are frequently habitats, and so intolerant to deforestation. Five other observed ranging in open landscape. If this condition is species (Myrmecophaga tridactyla, Ozotoceros bezoarticus, met, the species will typically show populations parameters Hydrochoerus hidrochaeris and Tamandua tetradactyla) like high densities within preferable habitats. Studies on have shown moderate dependence on arboreal/forest capybaras of the Pantanal show that the use of habitats habitats. Higher abundance of forested areas in a given varies seasonally (Alho et al., 1989; Alho, 2005a, 2008). study area in the Pantanal seems to favour the presence During the dry season, capybaras spend the night in the of jaguars (Azevedo and Murray, 2007). forest. In the early morning they leave the forest to graze on the grassland. During the rainy season, the capybaras 3.5. Semi-aquatic species also spend the night in the forest, but in the morning usually Mammals adapted for aquatic life in the Pantanal, with emerge and go directly to the water or to grazing areas. Use webbed feet, a dense underfur, short legs, a long body of aquatic and forest vegetation in their diet at that time and long tail, are two carnivore species belonging to the increases significantly, since few grazing areas re­main above family Mustelidae, the giant otter Pteronura brasiliensis water level. Group sizes ranged from 2 to 25 individuals, and the freshwater otter Lontra longicaudis. The capybara depending on the kind of preferable habitats. Each group is a semi-aquatic largest rodent, a keystone species of the occupied an area ranging from 33.67 to 196.04 ha. Home Pantanal. Another large mammal that frequently uses habitats range of a group contained foraging open area, a patch with presence of water is the tapir Tapirus terrestris. The of forest (usually a gallery forest or a patch of savanna, bush dog Speothos venaticus has a close association with locally known as capão de cerrado) and water (river, water, presenting morphological adaptation for swimming, corixo or baía). The densities in the most used habitats ranged from 0.01 to 0.69 capybara/ha. Each social group webbed feet. occupied a core area within its home range varying from Other mammal species with some association with 2.97 to 52.80 ha. water are marsupials, some confined to habitats of gallery Many aspects of the behaviour and ecology of the forest and other kinds of arboreal habitats with close relation capybara are affected by seasonal fluctuations in the amount to water such as rivers and corixos: Marmosa murina; of available food. Some preferred food items that are richer Micoureus constantiae and M. demerarae; Marmosops in protein tend to be more seasonal than poorer food items. noctivagus and Chironectes minimus. There is a period of the year, from June until November, Giant otter Pteronura brasiliensisis has a long and when the standing crop on lower areas susceptible to flattened tail, adapted for swimming. The fur is thick flooding is abundant and is consumed by capybaras. During and glossy. They are social animals, living in groups of the remainder of the year the presence of these food items 5-15 related individuals. They are highly vocal and their is very scarce. Thus, the times of food abundance and noise is easily recognised by riverine men in the Pantanal. scarcity are predicted by the flooding pattern. Capybara The social group moves according to movement of seasonal group size increases from the beginning (rainy season) water of the Pantanal, usually following school of fishes to the middle of the year (dry season). During the floods in movement. They pursue fish and hunt in groups. The the groups subdivide and are largely confined to the forest patches, while in the dry season more animals are observed giant otter is a semi-aquatic predator which relies mainly feeding on the pasture of the grassland (Alho et al., 1989; on fish, occurring in the Pantanal in habitats with slow Alho, 2005a, 2008; Mamede and Alho, 2006). moving waters (rivers, corixos and large permanent baías) The major part of the habitat heterogeneity observed presenting high productivity of fish. They are diurnal in an ecological community of the Pantanal is determined mammals and form cohesive social groups, moving in by vegetation, mainly the arboreal or forested habitat, that function of seasonal flooding. During the dry season the comprise a matrix of high complexity, forming different social groups occupy one stretch of the river, corixo or

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 297-310 301 Alho, CJR., Camargo, G. and Fischer, E. baía and actively scent mark the occupied territory also The threat status of this species is vulnerable, including using communal latrines. MMA ranking as well as IUCN category. All vegetation Different surveys have shown occurrence of giant otter communities in which marsh deer Blastocerus dichotomus in the Pantanal. The species is documented to occur (active have been observed (Tomás, 1993) are frequently flooded burrows with recent tracks and latrines) along 324 km of dur­ing the wet season (most habitats are formed by aquatic the Aquidauana river, between the town of Aquidauana plants). The vegetation type most used by marsh deer is and the village of Passo da Lontra, in Mato Grosso do Sul Andropogon grassland and other open areas are dominated state. The greater part of this river stretch is constituted by by Pontederia, Scleria, Nymphaea, Eleocharis, Thalia, the Aquidauana River (258 km), and the remaining 82 km Axonopus, Oryza, Nymphoides and Luziola communities. correspond to the Miranda River (Tomás et al., 2000). Marsh deer select about 35 plant species, mainly aquatic A study conducted at Vermelho and Miranda rivers plants. Pontederia cordata L. (including both flowers and leaves), Thalia geniculata L. (mainly flowers), Nymphaea in the Pantanal concluded that time spent by giant otters spp. L., Aeschynomene sensitiva Sw., A. fluminensisVell. marking varied between groups (Leuchtenberger and Mourão, Conc., Discolobium pulchellum Benth, Reussia spp. Endl., 2009): the alpha males marked more frequently (62% of Leersia hexandra Sw. and others are frequently eaten by marking events, 55 minutes) than the alpha females (17% of marsh deer. Tomás (1993) provides a list of those plants. marking events, 13.6 minutes). The study pointed out that Two canid species are in danger: the maned wolf and scent-marking among giant otter individuals within the the bush dog. The maned wolf - lobo-guará- Chrysocyon social group can play a relevant role in communication of brachyurus, inhabits the grasslands and scrub forest social and sexual status and territorial defense. of the Pantanal. It is listed as vulnerable by MMA and The freshwater otter Lontra longicaudis has a semi- near threatened by IUCN. Its population is experiencing aquatic habit since this species depends on the riverbanks, a continuing decline due to ongoing habitat loss and where they actively mark territories to rest and reproduce, degradation, road kills and other threats (Rodden et al., 2008). and the water to search for food. Estimated density in some The bush dog or cachorro-vinagre Speothos venaticus is Pantanal areas is of one individual for each 2-3 km along categorised as vulnerable. It is an intrinsically rare species the Negro river (Kruuk, 2006). They prefer clear running although having a wide distribution range, it is nowhere waters, protected by gallery forest, and river banks that abundant and occurs at very low densities. can provide shelters. They prey primarily on fish, being Bush dogs are habitat generalist, showing some observed alone or in small group, generally the female preference to areas near water. Survey on direct sightings and its young. and evidences of occurrence (feces, tracks, carcasses) recorded in a protected area of the Pantanal have shown 3.6. Threatened species a home-range size of 150 km² occupied by a group of Medium to large sized mammals (12 species), two bat six bush dogs (Lima et al., 2009). It was estimated the and rodent species of the Pantanal are considered threatened, presence of about five groups of bush dogs with sizes according to the Livro Vermelho da Fauna Brasileira varying from two to five individuals, but about two was the Ameaçada de Extinção (Brazilian Red Book of the Fauna average group size, although some isolated individuals were Threatened with Extinction) of the Ministério do Meio detected. This study identified the nine-banded armadillo Ambiente (Brazilian Ministry of the Environment) based Dasypus novemcinctus as the preferred prey of bush dogs. on documents published by IBAMA (Brazilian Institute of In forest habitats they create dens in burrows of old trees Environment and Renewable Natural Resources – Portaria where the female nurses its young. Nº. 62 in 1997), and by the Ministry (Instrução Normativa Threatened felid species of the Pantanal are: the ocelot Nº. 3 in 2003, and Instrução Normativa Nº. 5 in 2004) or jaguatirica, Leopardus pardalis mitis, listed by MMA (Table 1). Among bat species are Vampyrum spectrum as vulnerable; the little spotted cat or gato‑do‑mato- and Chiroderma doriae. Phyllomys brasiliensis is the only pequeno, Leopardus tigrinus, under the threat category of rodent occurring in the Pantanal redlisted as endangered vulnerable; the margay cat or gato-maracajá, Leopardus in both lists (MMA, 2008a,b; IUCN, 2011). Blastoceros wiedii, listed as vulnerable; the Pampas cat or gato‑palheiro, dichotomus, Chrysocyon brachyurus, Leopardus pardalis, Leopardus colocolo, also vulnerable; the puma or suçuarana Leopardus tigrinus , Leopardus wiedii, Myrmecophaga Puma concolor shows sympatric range with jaguar in the tridactyla, Leopardus colocolo, Panthera onca, Priodontes Pantanal (two subspecies are listed as vulnerable by MMA: maximus, Pteronura brasiliensis, Puma concolor, and P.c. capricornensis and P.c.greeni, both not occcurring Speothos venaticus are among medium-large sized mammals in the Pantanal); and the jaguar or onça, Panthera onca, listed in the Brazilian Red Book (Table 1), as well in the categorised as vulnerable. Among felid species, Leopardus IUCN Redlist, which some differences in the categories wiedii and Panthera onca are categorised as vulnerable (Table 1). by IUCN Red List. The marsh deer, cervo-do-pantanal, Blastocerus These species occur within the Pantanal habitats, dichotomus, is the largest Brazilian deer. Interdigital documented in different studies. Using capture-recapture membranes, extended hooves, and relatively long limbs are analysis, Trolle and Kéry (2005), estimated Leopardus adaptation features to flooding habitats (Tomás et al., 1997). pardalis density in a study area of 0.112 individuals

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Table 1. List of 174 mammal species occurring in the Pantanal floodplain, ordered from the most to the least speciose groups, based on published records. Extinction threatening status by the International Union for Conservation of Nature (IUCN) and the Livro Vermelho da Fauna Brasileira Ameaçada de Extinção (MMA, 2008) is given. ORDER Family IUCN IBAMA Species CHIROPTERA Phyllostomidae Anoura caudifer (E. Geoffroy, 1818) Anoura geoffroyi Gray, 1838 Artibeus cinereus (Gervais, 1856) Artibeus fimbriatusGray, 1838 Artibeus glaucus Thomas, 1893 Artibeus lituratus (Olfers, 1818) Artibeus obscurus (Schinz, 1821) Artibeus planirostris (Spix, 1823) Carollia brevicauda (Schinz, 1821) Carollia perspicillata (Linnaeus, 1758) Chiroderma doriae O. Thomas, 1891 Vu Chiroderma villosum Peters, 1860 Chrotopterus auritus (Peters, 1856) Desmodus rotundus (E. Geoffroy, 1810) Diaemus youngi (Jentink, 1893) Diphylla ecaudata Spix, 1823 Glossophaga soricina (Pallas, 1766) Glyphonycteris behnii (Peters, 1865) (= Micronycteris behnii) Lonchorhina aurita Tomes, 1863 Lophostoma brasiliense Peters, 1866 (= Tonatia brasiliense) Lophostoma silvicolum d’Orbigny, 1836 (= Tonatia silvicola) Macrophyllum macrophyllum (Schinz, 1821) Micronycteris megalotis (Gray, 1842) Micronycteris minuta (Gervais, 1856) Micronycteris sanborni Simmons, 1996 Mimon bennettii (Gray, 1838) Mimon crenulatum (E. Geoffroy, 1803) Phylloderma stenops Peters, 1865 Phyllostomus discolor Wagner, 1843 Phyllostomus elongatus (E. Geoffroy, 1810) Phyllostomus hastatus (Pallas, 1767) Platyrrhinus helleri (Peters, 1866) Platyrrhinus lineatus (E. Geoffroy, 1810) Pygoderma bilabiatum (Wagner, 1843) Sturnira lilium (E. Geoffroy, 1810) Tonatia bidens (Spix, 1823) Trachops cirrhosus (Spix, 1823) Uroderma bilobatum Peters, 1866 Uroderma magnirostrum Davis, 1868 Vampyressa pusilla (Wagner, 1843) Vampyrodes caraccioli (Thomas, 1889) Vampyrum spectrum (Linnaeus, 1758) Nt Molossidae

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Table 1. Continued... ORDER Family IUCN IBAMA Species Cynomops abrasus (Temminck, 1827) (= Molossops abrasus) Cynomops planirostris (Peters, 1865) (= Molossops planirostris) Eumops auripendulus (Shaw, 1800) Eumops bonariensis (Peters, 1874) Eumops glaucinus (Wagner, 1843) Eumops patagonicus Thomas, 1924 Eumops perotis (Schinz, 1821) Molossops temminckii (Burmeister, 1854) Molossus currentium (Thomas, 1901) (= M. bondae) Molossus molossus (Pallas, 1766) Molossus pretiosus Miller, 1902 Molossus rufus E. Geoffroy, 1805 (= M. ater) Nyctinomops aurispinosus (Peale, 1848) Nyctinomops laticaudatus (E. Geoffroy, 1805) Nyctinomops macrotis (Gray, 1840) Promops centralis Thomas, 1915 Promops nasutus (Spix, 1823) Vespertilionidae Eptesicus brasiliensis (Desmarest, 1819) Eptesicus furinalis (d’Orbigny, 1847) Histiotus velatus (I. Geoffroy, 1824) Lasiurus borealis (Muller, 1776) Lasiurus cinereus (Beauvois, 1796) Lasiurus ega (Gervais, 1856) Myotis albescens (E. Geoffroy, 1806) Myotis nigricans (Schinz, 1821) Myotis riparius Handley, 1960 Myotis simus Thomas, 1901 Emballonuridae Centronycteris maximiliani (Fischer, 1829) Peropteryx kappleri Peters, 1867 Peropteryx macrotis (Wagner, 1843) Rhynchonycteris naso (Wied-Neuwied, 1820) Saccopteryx bilineata (Temminck, 1838) Saccopteryx leptura (Schreber, 1774) Mormoopidae Pteronotus gymnonotus Natterer, 1843 Pteronotus parnellii (Gray, 1843) Pteronotus personatus (Wagner, 1843) Noctilionidae Noctilio albiventris Desmarest, 1818 Noctilio leporinus (Linnaeus, 1758) RODENTIA Cricetidae

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Table 1. Continued... ORDER Family IUCN IBAMA Species Akodon toba Thomas, 1921 Akodon varius Thomas, 1902 Calomys callosus (Rengger, 1830) Cerradomys scotti Langguth & Bonvicino, 2002 (= Oryzomys scotti) Cerradomys subflavus(Wagner, 1842) (= Oryzomys subflavus) Holochilus brasiliensis (Desmarest, 1819) Holochilus sciureus Wagner, 1842 Hylaeamys megacephalus (Fischer, 1814) (= Oryzomys megacephalus, O. capito) Kunsia tomentosus (Lichtenstein, 1830) Necromys lasiurus (Lund, 1841) (= Bolomys lasiurus) Nectomys squamipes (Brants, 1827) Oecomys bicolor (Thomas, 1860) Oecomys concolor (Wagner, 1845) (= Oryzomys concolor) Oecomys mamorae (Thomas, 1906) Oecomys roberti (Thomas, 1904) Oligoryzomys chacoensis (Myers & Carleton, 1981) Oligoryzomys fornesi (Massoia, 1973) Oligoryzomys microtis (Allen, 1916) Oligoryzomys nigripes (Olfers, 1818) Echimyidae Clyomys laticeps (Thomas, 1909) Phyllomys brasiliensis Lund, 1839 (= Echimys brasiliensis) En En Proechimys longicaudatus (Rengger, 1830) Thrichomys apereoides (Lund, 1839) Thrichomys pachyurus (Wagner, 1845) Caviidae Cavia aperea Erxleben, 1777 Galea musteloides Meyen, 1832 Hydrochoerus hydrochaeris (Linnaeus, 1766) Dasyproctidae Dasyprocta azarae Lichtenstein, 1823 Dasyprocta punctata Gray, 1842 Sciuridae Guerlinguetus ignitus (Gray, 1867) (= Sciurus ignitus) Urosciurus spadiceus Olfers, 1818 (= Sciurus spadiceus) Cuniculidae Cuniculus paca (Linnaeus, 1766) (= Agouti paca) Erethizontidae Coendou prehensilis (Linnaeus, 1758) CARNIVORA Felidae Leopardus colocolo (Molina, 1782) (= Oncifelis colocolo, L. braccatus) Nt Vu Leopardus geoffroyi (d ‘Orbigny & Gervais, 1844) (= Oncifelis geoffroyi) Nt Leopardus pardalis (Linnaeus, 1758) Vu Leopardus tigrinus (Schreber, 1775) Vu Vu

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Table 1. Continued... ORDER Family IUCN IBAMA Species Leopardus wiedii (Schinz, 1821) Nt Vu Panthera onca (Linnaeus, 1758) Nt Vu Puma concolor (Linnaeus, 1771) Vu Puma yagouaroundi (E. Geoffroy, 1803) (= Herpailurus yagouaroundi) Mustelidae Eira barbara (Linnaeus, 1758) Galictis cuja (Molina, 1782) Galictis vittata (Schreber, 1776) Lontra longicaudis (Olfers, 1818) Pteronura brasiliensis (Gmelin, 1788) En Vu Canidae Cerdocyon thous (Linnaeus, 1766) Chrysocyon brachyurus (llliger, 1815) Nt Vu Lycalopex vetulus (Lund, 1842) Speothos venaticus (Lund, 1842) Nt Vu Procyonidae Nasua nasua (Linnaeus, 1766) Procyon cancrivorus (G.[Baron] Cuvier, 1798) Mephitidae Conepatus semistriatus (Boddaert, 1785) DIDELPHIMORPHIA Didelphidae Caluromys lanatus (Olfers, 1818) Caluromys philander (Linnaeus, 1758) Chironectes minimus (Zimmermann, 1780) Cryptonanus chacoensis (Tate, 1931) (= Gracilinanus chacoensis) Didelphis albiventris Lund, 1840 Didelphis marsupialis (Linnaeus, 1758) Gracilinanus agilis (Burmeister, 1854) Lutreolina crassicaudata (Desmarest, 1804) Marmosa murina (Linnaeus, 1758) Marmosops noctivagus (Tschudi, 1844) Marmosops ocellatus (Tate, 1931) Metachirus nudicaudatus (E. Geoffroy, 1803) Micoureus constantiae (Thomas, 1904) Micoureus demerarae (Thomas,1905) Monodelphis brevicaudata (Erxleben, 1777) Monodelphis domestica (Wagner, 1842) Philander opossum (Linnaeus 1758) Thylamys macrurus (Olfers, 1818) Nt CINGULATA Dasypodidae Cabassous chacoensis Wetzel, 1980 Nt Cabassous tatouay (Desmarest, 1804) Cabassous unicinctus (Linnaeus, 1758) Dasypus novemcinctus Linnaeus, 1758 Dasypus septemcinctus Linnaeus, 1758

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Table 1. Continued... ORDER Family IUCN IBAMA Species Euphractus sexcinctus (Linnaeus, 1758) Priodontes maximus (Kerr, 1792) Vu Vu Tolypeutes matacus (Desmarest, 1804) Nt ARTIODACTYLA Cervidae Blastocerus dichotomus (Illiger, 1815) Vu Vu Mazama americana (Erxleben, 1777) Mazama gouazoubira (Fischer, 1814) (= M. gouazoupira) Ozotoceros bezoarticus (Linnaeus, 1758) Nt Tayassuidae Pecari tajacu (Linnaeus, 1758) Tayassu pecari (Link, 1795) Nt PRIMATES Cebidae Cebus apella (Linnaeus, 1758) (= C. cay) Mico melanurus (E. Geoffroy in Humboldt, 1812) (= Callithrix melanura) Aotidae Aotus azarae (Humboldt, 1811) Atelidae Alouatta caraya (Humboldt, 1812) Pitheciidae Callicebus donacophilus (d’Orbigny, 1836) PILOSA Myrmecophagidae Myrmecophaga tridactyla Linnaeus, 1758 Nt Vu Tamandua tetradactyla (Linnaeus, 1758) LAGOMORPHA Leporidae Sylvilagus brasiliensis (Linnaeus, 1758) PERISSODACTYLA Tapiridae Tapirus terrestris Linnaeus, 1758 Vu

per km². Soisalo and Cavalcanti (2006), studying jaguars giant otter or ariranha, Pteronura brasiliensis, is also in the Pantanal, found densities ranging from 6.6 to categorised as vulnerable by MMA, and as endangered 11.7 jaguars/100 km², depending on the survey method by IUCN (see 3.4 Semi-aquatic species). employed. They successfully tested the suitability of In addition to Brazilian legislation on endangered camera-trap capture-recapture sampling methods combined wildlife, there are international organisations dealing with telemetry technology for monitoring the status of with trade of wild species CITES (1979) (Convention jaguars in an open wet grassland habitat of the Pantanal. on International Trade in Endangered Species of Flora In a study area of the Pantanal, a jaguar density ranging and Fauna- Convenção sobre o Comércio Internacional from 6.5 to 6.7 individuals per 100 km² was estimated das Espécies da Flora e da Fauna Selvagens em Perigo (Trolle and Kéry, 2005). de Extinção) which Brazil has been a part of since 1975- The giant-armadillo - tatu-canastra- Priodontes maximus Dec. nº 76.623/75; conservation and Red List or Red Data is the largest nocturnal and fossorial living armadillo, List on endangered species - IUCN (2011) (International occurring in the Pantanal. Its threatened category is Union for Conservention of Nature - União Internacional vulnerable in the MMA and IUCN lists. The semi-aquatic para Conservação da Natureza e dos Recursos Naturais);

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 297-310 307 Alho, CJR., Camargo, G. and Fischer, E. knowledge, conservation and sustainable use of biodiversity structure and function. If any one or more of the conditions (Convention on Biological Diversity - Convenção sobre needed for a healthy mammalian community is missing, Diversidade Biológica) (CBD, 1992) and others. for example, absence of an arboreal or forested area due to 3.7. Response of mammals to seasonal flooding conversion of local vegetation into pasture, it can cause a chain reaction affecting mammalian population parameters, Mammals respond to seasonal shrinking-and-expansion of community structure and behavioural ecology for feeding habitats due to flooding regime of the Pantanal with highest and reproductive niches. Human activities are increasing abundance of species observed during the dry season (August the vulnerability of the natural habitats of the Pantanal. and September), when there is a considerable expansion Changes brought about by people have caused habitat loss of terrestrial habitats, mainly seasonally flooded grassland and alteration, more erosion and sedimentation, pollution, (Mamede and Alho, 2006). Animal abundance (in terms of observed individual frequencies) varied during the dry unusual flooding and droughts. and wet seasons and the seasonally flooded grassland was Large-scale habitat disturbances, such as the use of fire the most utilised habitat by mammals in the dry season. and the conversion of natural vegetation into pasture or Recurrent shallow flooding occupies 80% of the soybean plantations, have the potential to alter population Pantanal; during the dry season flooded areas dry up. parameters, community structure, use of space and other Fluctuating water levels, nutrients and wildlife form a ecological requirements of mammal assemblages. Patches of dynamic ecosystem. A total of 36 species were observed cerrado (capões de cerrado) and cerradão on cordilheiras, in the field. The capybara Hydrochoerus hydrochaeris was for example, are rapidly disappearing as natural vegetation the most frequent species, followed by the crab-eating‑fox is converted into agricultural land or pastures for cattle Cerdocyon thous and the marsh deer Blastocerus dichotomus ranching. Such environmental alterations can damage (Mamede and Alho, 2006). mammal habitat specialists and benefit pan-habitat species, A study scanning multichannel microwave radiometres changing community composition associated with pristine to reveal inundation patterns in the Pantanal showed habitat gradients in the Pantanal landscape. maximum inundation occurring as early as February in the Although the Pantanal is rich in wildlife diversity and northern sub-regions and as late as June in the south, as a its habitats are still in good conservation status, about result of the delayed drainage of the region (Hamilton et al., 95% of its area is still privately owned, with livestock 1996). An area of 131,000 km2 was inundated annually being the main economic activity. However, in addition to during nine years of observation, between 1979 and 1987. increasing habitat loss and alteration due to deforestation, 2 An average area of 53,000 km is inundated annually and illegal hunting, overfishing, pollution like sewage from monthly estimates of the total area inundated range from urban areas, erosion with sedimentation of river beds, 2 11,000 to 110,000 km . and control of jaguars related to livestock activity are There is observed evidence that seasonal habitat significant signs of human occupation, bringing wildlife availability of the Pantanal influences population parameters and humans into direct conflict. of mammal species. By comparing observed frequencies of animals in the survey transects, a frequency analysis Acknowledgements – Cleber Alho has conducted research in was applied to check the difference of habitat utilisation the Pantanal for over two decades and statements provided here by the species showed statistically significant differences reflect this field experience. Celina Alho helped elaborating the manuscript. We thank Susan Casement for valuable language among the observed habitats - seasonally flooded grassland, revision and comments. Financial support to G. Camargo was patches of Cerrado, gallery forest and mesophytic forest provided by CAPES and to E. Fischer by CNPq. and the seasonally flooded grassland was the most utilised habitat by the species, followed by the mesophytic forest References and gallery forest . Thus, there is a significant association of species utilisation and type of available seasonal habitat Agência Nacional de Águas – ANA, 2004. Strategic action (Mamede and Alho, 2006). Additionally, the distribution program for the integrated management of the Pantanal and the of the marsh deer in the Pantanal varies as a function of Upper Paraguay River Basin. Brasília, DF: ANA/GEF/PNUMA/ seasonal floods (Tomás et al., 2001). OEA. 315 p. 3.8. Concluding remarks: conservation implications ALHO, CJR., coord., 2000. Fauna silvestre da região do rio The terrestrial and aquatic habitats used by the Pantanal Manso – MT. Brasília: Ministério do Meio Ambiente. 268 p. mammals have been selected over an evolutionary scale Edições Ibama e Eletronorte. by the rhythm of annual flooding in the wet season and -, 2003. Capybaras (entry of an encyclopedia). In KLEIMAN, retraction of the water to river valleys in the dry season. DG., GEIST, V., HUTCHINS, M. and MCDADE, MC., Org. Among more than 170 mammals species (see Table 1) Grzimek’s Animal Life Encyclopedia - Mammals V. Farmington distributed in the Pantanal’s habitats, there are 14 species Hills, Michigan: Gale Group. vol. 16, p. 401-406. officially listed as in danger. In natural habitats of the -, 2005a. The Pantanal. In FRASER, LH. and KEDDY, PA., Org. Pantanal, the interacting effects of multiple ecological The World’s Largest Wetlands – Ecology and Conservation. New processes determine the health of mammalian community York, USA: Cambridge University Press. p. 203-271.

308 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 297-310 Pantanal mammals

-, 2005b. Intergradation of habitats of non-volant small mammals HAMILTON, SK., SIPPEL, SJ. and MELACK, JM., 1996. in the patchy Cerrado landscape. Arquivos do Museu Nacional Inundation patterns in the Pantanal wetland of South America do Rio de Janeiro, vol. 63, p. 41-48. determined from passive microwave remote sensing. Archives of Hydrobiology, vol. 137, p. 1-23. -, 2008. Biodiversity of the Pantanal: response to seasonal flooding regime ant to environmental degradation. Revista Brasileira HARRIS, MB., TOMÁS, WM., MOURÃO, G., SILVA, CJ., de Biologia = Brazilian. Journal of Biology, vol. 68, no. 4, GUIMARÃES, E., SONODA, F. and FACHIN, E., 2005. p. 957‑966. Suppl. Safeguarding the Pantanal Wetlands: threats and conservation iniciatives. Conservation Biology, vol. 19, no. 3, p. 714-720. ALHO, CJR., CAMPOS, ZMS. and GONÇALVES, HC., 1989. Ecology, Social Behavior, and Management of the Capybara International Union for Conservation of Nature – IUCN, 2011 (Hydrochaeris hydrochoeris) in the Pantanal of Brazil. In Redlist. Available from: . Mammalogy. Gainesville: Sandhill Crane Press, University of . p. 163-194. KRUUK, H., 2006. Otter: ecology, behaviour and conservation. N.Y.: Oxford University Press, 261 p. ALHO, CJR., LACHER Jr., TE., CAMPOS, JMS. and GONÇALVES, HC., 1988. Mamíferos da Fazenda Nhumirim, sub-região de LACHER Jr., TE. and ALHO, CJR., 1989. Microhabitat use Nhecolândia, Pantanal do Mato Grosso do Sul: Levantamento among small mammals in the Brazilian Pantanal. Journal of preliminar de espécies. Revista Brasileira de Biologia = Brazilian Mammalogy, vol. 70, no. 2, p. 396-401. Journal of Biology, vol. 48, no. 2, p. 213-225. -, 2001. Terrestrial small mammal richness and habitat associations ALHO, CJR., STRUSSMANN, C., VOLPE, M., SONODA, F., in an Amazon forest-Cerrado contact zone. Biotropica, Storrs, MARQUES, AAB., SCHNEIDER, M., SANTOS-JUNIOR, TS. and vol. 33, no. 1, p. 171-181. MARQUES, SR., 2003. Conservação da Biodiversidade da Bacia LEUCHTENBERGER, C. and MOURÃO, G., 2009. Scent‑Marking do Alto Paraguai. Campo Grande – MS: Ed. UNIDERP. 466 p. of Giant Otter in the Southern Pantanal, Brazil. Ethology, ARAGONA, M. and MARINHO-FILHO, J., 2009. História vol. 115, no. 3, p. 210-216. natural e biologia reprodutiva de marsupiais no Pantanal, Mato LIMA, ES., JORGE, RSP., DALPONTE, JC., 2009. Habitat Grosso, Brasil. Zoologia, vol. 26, no. 2, p. 220-230. use and diet of bush dogs, Speothos venaticus, in the Northern AZEVEDO, FCC. and MURRAY, DL., 2007. Spatial organization Pantanal, Mato Grosso, Brazil. Mammalia, vol. 73, no. 1, p. 13-19. and food habits of jaguars (Panthera onca) in a floodplain forest. LONGO, JM., FISCHER, E., CAMARGO, G. and SANTOS, Biological Conservation, vol. 137, p. 391-402. CF., 2007. Occurrence of Vampyressa pusilla Chiroptera, BONVICINO, C. and LACHER, T., 2008. Thrichomys pachyurus. Phyllostomidae) in Southern Pantanal. Biota Neotropica, vol. 7, In IUCN 2009. IUCN Red List of Threatened Species. Version no. 3. Availabre from: . Access in: pt/abstract?short-communication+bn02407032007>. 10 mar. 2010. MAMEDE, SB. and ALHO, CJR., 2006. Response of wild CÁCERES, NC., CARMIGNOTTO, AP., FISCHER, E. and mammals to seasonal shrinking-and-expansion of habitats due SANTOS, CF., 2008. Mammals from Mato Grosso do Sul, Brazil. to flooding regime of the Pantanal, Brazil. Revista Brasileira de Check List, vol. 4, no. 3, p. 321-335. Biologia = Brazilian Journal of Biology, vol. 66, no. 4, p. 991-998. CAMARGO, G. and FISCHER, E., 2005. Primeiro registro MARINHO FILHO, J., Org., 2007. Mastofauna do Cerrado e do morcego Mimon crenulatum (Phyllostomidae) no Pantanal, Pantanal - diversidade e conservação. In: Cerrado e Pantanal sudoeste do Brasil. Biota Neotropica, vol. 5, no. 1. Available áreas e ações prioritárias para conservação da biodiversidade. from: . Biodiversidade, no. 17. CARMIGNOTTO, AP., 2004. Pequenos mamíferos terrestres do MARINHO-FILHO, J. and SAZIMA, I., 1998. Brazilian bats bioma Cerrado: padrões faunísticos locais e regionais. São Paulo: and conservation biology: a first survey. In KUNZ, TH. and Universidade São Paulo. 404 p. Doctoral thesis. RACEY, PA., Ed. Bat biology and conservation. Washington D.C.: Smithsonisn Institution Press. p. 282-294. CARMIGNOTTO, AP. and MONFORT, T., 2006. and distribution of the Brazilian species of Thylamys (Didelphimorphia: MAURO, RA., MOURÃO, GM., COUTINHO, ME., SILVA, Didelphidae). Mammalia, vol. 70, p. 126-144. MP. and MAGNUSSON, WE., 1998. Abundance and distribution of marsh deer Blastocerus dichotomus (Artiodactyla: Cervidae) Convention on Biological Diversity – CBD, 1992. The Convention. in the Pantanal, Brazil. Revista de Ecología Latinoamericana, Available from: . vol. 5, no. 1-2, p. 13-20. Convention on International Trade in Endangered Species of Ministério do Meio Ambiente – MMA, 2008a. Livro vermelho Flora and Fauna – CITES, 1979. Text of the Convention. Available da fauna brasileira ameaçada de extinção. Brasília, DF. vol. 1, from: . 511 p. Series Biodiversidade, vol. 19. COUTINHO, ME., CAMPOS, ZMS., MOURÃO, GM. and -, 2008b. Livro vermelho da fauna brasileira ameaçada de extinção. MAURO, RA., 1997. Aspectos ecológicos dos vertebrados Brasília, DF. vol. 2, 907 p. Series Biodiversidade, vol. 19. terrestres e semi-aquáticos no Pantanal. In Brasil. Ministério do Meio Ambiente, dos Recursos Hídricos e da Amazônia Legal. Plano MOURÃO, G., COUTINHO, M., MAURO, R., CAMPOS, Z., de conservação da Bacia do Alto Paraguai (Pantanal) – PCBAP: TOMAS, W. and MAGNUSSON, W., 2000. Aerial surveys of diagnóstico dos meios físicos e bióticos: meio biótico. Brasília. caiman, marsh deer and pampas deer in the Pantanal Wetland of vol. 2, no. 3, p. 183-322. Brazil. Biological Conservation, vol. 92, p. 175-183.

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 297-310 309 Alho, CJR., Camargo, G. and Fischer, E.

OLIVEIRA, JA., PESSÔA, LM., OLIVEIRA, LFB., ESCARLATE, TEIXEIRA, RC., CORREA, CE. and FISCHER, E., 2009. F., CARAMASCHI, FP., LAZAR, A. and CORDEIRO, JLP., Frugivory by Artibeus jamaicensis (Phyllostomidae) bats in the 2002. Mamíferos da RPPN Sesc Pantanal. In Conhecendo o Pantanal, Brazil. Studies on Neotropical Fauna and Environment, Pantanal. Várzea Grande, MT, Brasil. p. 33-38. Divulgação de vol. 44, no. 1, p. 7-15. Pesquisa, no. 1. TOMÁS, WM., 1993. Status and Ecology of a Marsh Deer REIS, NR., PERACCHI, AL., PEDRO, WA. and LIMA, IP., (Blastocerus dichotomus) population in southern Pantanal, Brazil. Ed., 2006. Mamíferos do Brasil. Londrina, PR, Brasil: Biblioteca Brasília. WWF-Brasil. Unpublished report. Central da Universidade Estadual de Londrina. 437 p. TOMÁS, WM., BECCACECI, MD. and PINDER, L., 1997. RODDEN, M., RODRIGUES, F. and BESTELMEYER, S., Cervo‑do-Pantanal. In DUARTE, JMB., Ed. Biologia e conservação 2008. Chrysocyon brachyurus. In IUCN 2010. IUCN Red de cervídeos sul-americanos: Blastocerus, Ozotoceros e Mazama. List of Threatened Species. Version 2010.1. Available from: Jaboticabal, SP, Brasil: FUNEP. p. 24-38. . Access in: 13 mar. 2010. TOMÁS, WM., BORGES, PAL., ROCHA, HJF., SÁ-FILHO, R., RODRIGUES, FHG., MEDRI, IM., TOMÁS, WM. and MOURÃO, KUTCHENSKI-JÚNIOR, F., and UDRY, TV., 2000. Potencial GM., 2002. Revisão do conhecimento sobre ocorrência e distribuição dos rios Aquidauana e Miranda, no Pantanal de Mato Grosso do de Mamíferos do Pantanal. Embrapa Pantanal. 41 p. Documentos, no. 38. Sul, para a conservação da ariranha (Pteronura brasiliensis). In III Simpósio sobre Recursos Naturais e Sócio-econômicos do Pantanal. SABINO, J. and PRADO, PI., 2006. Síntese do conhecimento da Os Desafios do Novo Milênio.27-30 nov. 2000, Corumbá, MS. diversidade biológica de vertebrados do Brasil. In: LEVINSOHN, T., Org. Avaliação do estado do conhecimento da diversidade TOMÁS, WM., CÁCERES, NC., NUNES, AP., FISCHER, E., brasileira. Brasília, DF: Ministério do Meio Ambiente. vol. 2, MOURÃO, GM. and CAMPOS, Z. 2010. Mammals in the Pantanal p. 55-143. wetland, Brazil. In JUNK, WJ., SILVA, CJ., CUNHA, CN. and WANTZEN, KM., Org. The Pantanal: ecology, biodiversity and SANTOS, CF., NOGUEIRA, M., CUNHA, N., CARVALHO, LF. sustainable management of a large neotropical seasonal wetland. and FISCHER, E., 2010. Southernmost record of the Sanborn’s Sofia: Pensoft Publishers p. 127-141. big-eared bat, Micronycteris sanborni (Chiroptera, Phyllostomidae). Mammalia, vol. 74, p. 457-460. TOMÁS, WM., SALIS, SM., MOURÃO, GM. and SILVA, MP., 2001. Marsh deer (Blastocerus dichotomus) distribution SCHALLER, GB., 1983. Mammals and their biomass on a as a function of floods in the Pantanal wetland, Brazil. Studies Brazilian ranch. Arquivos de Zoologia, vol. 31, no. 1, p. 1-36. on Neotropical Fauna and Environment, vol. 36, no. 1, p. 9-13. SCHALLER, GB. and VASCONCELOS, JMC., 1978. A marsh TROLLE, M., 2003. Mammal survey in Western Pantanal. deer census in Brazil. Orix, vol. 14, p. 345-351. Biodiversity and Conservation, vol. 12, p. 823-826. SILVA, JSV. and ABDON, MM., 1998. Delimitação do Pantanal Brasileiro e suas Sub-regiões. Pesquisa Agropecuária Brasileira, TROLLE, M. and KÉRY, M., 2005. Camera-trap study of ocelot vol. 33, no. especial, p. 1703-1711. and other secretive mammals in the northern Pantanal. Mammalia, vol. 69, no. 3-4, p. 409-416. SILVA, JSV., ABDON, MM., BOOK, A. and SILVA, MP., 1998. Fitofisionomias dominantes em parte das sub-regiões do WILLIG, MR., PRESLEY, SJ., OWEN, RD. and LOPEZ- Nabileque e Miranda, sul do Pantanal. Pesquisa Agropecuária GONZALEZ, C., 2000. Composition and structure of bat Brasileira, vol. 33, no. especial, p. 1713-1720. assemblages in Paraguay: A subtropical-temperate interface. Journal of Mammalogy, vol. 81, p. 386-401. SOISALO, MK. and CAVALCANTI, SMC., 2006. Estimating the density of a jaguar population in the Brazilian Pantanal using WILSON, DE. and REEDER, DM., Eds., 2005. Mammal species camera-traps and capture–recapture sampling in combination with of the world. A taxonomic and geographic reference. 3rd ed. Johns GPS radio-telemetry. Biological Conservation, vol. 129, p. 487-496. Hopkins University Press. 2142 p.

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Biol., 2011, vol. 71, no. 1 (suppl.), p. 297-310 Bat-species richness in the Pantanal floodplain and its surrounding uplands Alho, CJR.a*, Fischer, E.b*, Oliveira-Pissini, LF.c* and Santos, CF.d* aPrograma de Pós-graduação em Meio Ambiente e Desenvolvimento Regional, Universidade Anhanguera – Uniderp, CEP 79037-280, Campo Grande, MS, Brazil bDepartamento de Biologia, Centro de Ciências Biológicas e da Saúde – CCBS, Universidade Federal de Mato Grosso do Sul – UFMS, CEP 79070-900, Campo Grande, MS, Brazil cPrograma de Pós-graduação em Meio Ambiente e Desenvolvimento Regional, Universidade Anhanguera – Uniderp, CEP 79037-280, Campo Grande, MS, Brazil dPrograma de Pós-graduação em Ecologia e Conservação, Centro de Ciências Biológicas e da Saúde – CCBS, Universidade Federal de Mato Grosso do Sul – UFMS, CEP 79070-900, Campo Grande, MS, Brazil *e-mail: [email protected], [email protected], [email protected], [email protected] Received October 14, 2010 – Accepted December 13, 2010 – Distributed April 30, 2011 (With 5 figures) Abstract We studied the bat fauna of the Pantanal floodplain and its surrounding plateaus in Mato Grosso do Sul, Brazil, based on the scientific collection atUniversidade Anhanguera – Uniderp and on the Projeto Morcegos do Pantanal data bank at UFMS, comprising 9,037 captures of 56 species recorded from 1994 to 2007. The Pantanal surveys were carried out in the Nhecolândia, Aquidauana, Miranda, and Paraguai sub-regions; the uplands surveys took place in the Maracaju, Bodoquena, and Urucum formations. Bat specimens were mist-netted over 376 nights in 35 sites, predominantly near fruiting trees, bat shelters, and forest patches. In the floodplain 46 species were recorded (n = 6,292 individuals), and 44 species were found in the uplands (n = 2,745 individuals). Six families were recorded: Phyllostomidae (30 species), Molossidae (12 species), Verpertilionidae (nine species) Noctilionidae (two species), Emballorunidae (two species) and Mormoopidae (one species). The bat fauna was predominantly composed of insectivore (32) and frugivore (15) species. The frugivorous Artibeus planirostris (n = 3,101 individuals) was the commonest species in floodplain and uplands. Other common species were Myotis nigricans (n = 762), Molossus molossus (n = 692), Noctilio albiventris (n = 681), Platyrrhinus lineatus (n = 633), Sturnira lilium (n = 461), Carollia perspicillata (n = 451), Glossophaga soricina (n = 436), Artibeus lituratus (n = 320), and Desmodus rotundus (n = 281). In the floodplain there were three insectivores among the most common species, contrasting with the uplands dominated by the frugivores. The diversity for the 35 sites assembled (H’ = 2.5) is comparable to that recorded for tropical forests. The bat fauna presented here represents 34% of the Brazilian bat species, and 62% of species reported for the Upper Paraguay River Basin. Additionally, five species are reported for the first time in Mato Grosso do Sul. Keywords: bats, biodiversity, Chiroptera, habitats, Pantanal. Riqueza de espécies de morcegos no Pantanal e no planalto em seu entorno Resumo Estudamos a fauna de morcegos na planície do Pantanal e nos planaltos de entorno no Mato Grosso do Sul, Brasil, com base na coleção científica daUniversidade Anhanguera – Uniderp e no banco de dados do Projeto Morcegos do Pantanal, UFMS, incluindo 9.037 capturas de 56 espécies, entre 1994 e 2007. Amostragens no Pantanal foram feitas nas sub-regiões da Nhecolândia, Aquidauana, Miranda e Paraguai; no planalto as amostragens foram realizadas nas formações de Maracaju, Bodoquena e Urucum. Espécies de morcegos foram registradas ao longo de 376 noites em 35 sítios, predominantemente com o uso de redes de neblina próximas a árvores frutíferas, abrigos e florestas. Na planície, foram registradas 46 espécies (n = 6.292 indivíduos) e no planalto 44 espécies (n = 2.745 indivíduos). Seis famílias foram encontradas: Phyllostomidae (30 espécies), Molossidae (12 espécies), Verpertilionidae (nove espécies), Noctilionidae (duas espécies), Emballorunidae (duas espécies) e Mormoopidae (uma espécie). A fauna de morcegos foi predominantemente composta de espécies insetívoras (32) e frugívoras (15). O frugívoro Artibeus planirostris (n = 3.101) foi a espécie mais comum na planície e no planalto. Outras espécies comuns foram Myotis nigricans (n = 762), Molossus molossus (n = 692), Noctilio albiventris (n = 681), Platyrrhinus lineatus (n = 633), Sturnira lilium (n = 461), Carollia perspicillata (n = 451), Glossophaga soricina (n = 436), Artibeus lituratus (n = 320) e Desmodus rotundus (n = 281). Na planície, ocorreram três espécies de morcegos insetívoros dentre as espécies mais comuns, contrastando com o planalto, onde houve dominância de frugívoros. A diversidade para os 35 sítios reunidos (H’ = 2,5) é comparável à encontrada em florestas tropicais. A fauna de morcegos apresentada aqui representa 34% das espécies brasileiras, e 62% das espécies já reportadas para a Bacia do Alto Paraguai. Adicionalmente, cinco espécies são reportadas pela primeira vez no Mato Grosso do Sul. Palavras-chave: morcegos, biodiversidade, quirópteros, hábitats, Pantanal.

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1. Introduction Cerrado plateaus, as well as to discuss the present status of natural habitat conservation and their bat-associated species. Bats are often the most species-rich mammalian taxonomic group in the tropics (Patterson et al., 2001) 2. Methods and represent nearly one-third of Brazilian land fauna (Marinho-Filho and Sazima, 1998). Different studies 2.1. Study sites have shown latitudinal gradients contributing to the understanding of geographic distribution of bat diversity, 2.1.1. Pantanal flood plain and surrounding uplands by analysis of species richness patterns on a large scale, The maze of fluctuating water levels, nutrients, and across wide spatial areas or with regional focus (Rohde, biota in the Pantanal forms a dynamic ecosystem (Alho, 1992; Willig, 2000; Stevens and Willig, 2002). Another 2008). The degree of inundation creates a range of major approach is to examine changes in species richness habitats. Flooding occupies about 80% of the whole along environmental gradients, when an assemblage of Pantanal. In contrast, during the dry season, most of the interacting bat species utilizes the same resource, for flooded areas stay dry, when the water returns to the example seasonal productivity, which is carried out on river beds or evaporates. Major habitats include patches smaller spatial scales (Alho, 2008; Drobner et al., 1998; (~ 0.5-5 ha) of semi-deciduous forests (capões) surrounded Wilsey and Potvin, 2000). Some environmental factors limit by grasslands, belts of cerradão or semi-deciduous forests the occurrence and abundance of some species, including surrounding lagoons (cordilheiras), riparian semi-deciduous habitat heterogeneity, seasonality and conservation status forests, and mono-specific forests of woody species such (Alho, 2005; Keddy et al., 2009). as Tabebuia aurea (paratudal) and Vochysia divergens Bat communities exhibit a variety of functional groups (cambarazal) (Silva et al., 2000; Araújo and Sazima, (guilds) such as insectivores, frugivores, nectarivores, 2003). The upper ground (where there are capões and sanguivores and piscivores (Stevens and Willig, 2002). cordilheiras) is at most only a couple of metres above Some studies have shown these bat assemblages in different average water level. Rivers and depressions locally known areas: trophic relations in the Phyllostomidae from Panga as corixos are lined by riparian forests. In these forest Reserve, southeastern Brazil (Pedro and Taddei, 1997); habitats, different species of Ficus and other trees serve bat community structure in a south-east Brazilian reserve as food supply and shelter for frugivores (Teixeira et al., in a transition zone between Cerrado and Atlantic Forest 2009). The uplands surrounding the Pantanal are covered (Falcão et al., 2003); diversity of a Cerrado habitat in by senso strictu cerrado, cerradão and semi-deciduous central Brazil (Zortéa and Alho, 2008). Recent literature forests, which are severely threatened by agriculture and has synthesised the number of species and distribution in cattle ranching (Alho, 2008; Scariot et al., 2005). Bats Brazil (Reis et al., 2007), as well as a bat community in a were sampled in 35 sites in the Pantanal floodplain and savanna habitat in Bolivia, near the Pantanal (Willig et al., its bordering plateaus, as described below. 2000; Aguirre, 2002). Available data on bats of the Pantanal floodplain and its neighbouring uplands, particularly from 2.1.2. Pantanal sampling sites Mato Grosso do Sul state, are reported in Leite et al. Field work was carried out in 19 sites (Figure 1) in (1998, 2000), Taddei et al. (2000, 2001, 2003), Camargo different Pantanal sub-regions and municipalities (see Silva and Fischer (2005), Gonçalves et al. (2007), Longo et al. and Abdon, 1998). In the Pantanal sub-region of Pantanal da (2007), Camargo et al. (2009), Cunha et al. (2009), and Nhecolândia eight sites were sampled: Fazenda Nhumirim Teixeira et al. (2009). (18° 59’ 6.93” S and 56° 37’ 24.37” W), Fazenda Arara Large and environmentally heterogeneous wetlands like Azul (19° 23’ 41.37” S and 57° 1’ 43.11” W), Fazenda the Pantanal (147,574 km² - latitude 15° 30’-22° 30’ S and Guanabara (18° 14’ 6.5” S and 55° 45’ 0.9” W), Fazenda longitude 54° 45’-58° 30’ W), exhibiting annual changes in Campo Neta (18° 45’ 38.8” S and 56° 17’ 48.3” W), Fazenda evenness along environmental gradients, play an important Santa Terezinha (19° 22’ 38.5” S and 56° 3’ 20.5” W), role in biological diversity, because of the heterogeneity Fazenda Baía das Pedras (19° 18’ 9.78” S and 55° 47’ of natural habitats, offering opportunities for feeding and 0.44” W), Fazenda Mangabal (19° 2’ 27.91” S and 55° reproductive niches (Alho, 2008; Keddy et al., 2009). 49’ 43.97” W), and Fazenda Barra Mansa (19° 36’ 0.94” S Differences in bat species abundance may respond to and 56° 4’ 36.31” W). In the sub-region of Pantanal de local environmental annual changes or to degree of habitat Aquidauana seven sites were sampled: Fazenda Conquista degradation. Because the Pantanal and its surrounding (19° 18’ 15.54” S and 55° 14’ 40.38” W), Fazenda Santa habitats harbour a large number of bat species, some Maria (19° 19’ 47.48” S and 55° 22’ 50.62” W), Fazenda common (high abundance) and some relatively rare, Olhos D’água (19° 26’ 0.52” S and 55° 12’ 8.71” W), intensive survey efforts are needed to estimate confidently Fazenda Santa Emília (19° 30’ 23.24” S and 55° 36’ the species abundance distributions. 46.10” W), Estância Caiman (19° 57’ 56’’ S and 56° 18’ The aim of this study is to show the magnitude of the 37’’ W), Fazenda Guaicurus (20° 4’ 49.96” S and 56° 28’ bat species richness and the structure of the community, 55.05” W), and Fazenda Santana (19° 37’ 51’’ S and 55° evaluating relative abundance and trophic distribution within 40’ 36’’ W). In the sub‑region of Pantanal do Miranda the Pantanal floodplain and throughout its surrounding three sites were sampled: Fazenda São Bento (19° 33’

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Figure 1. Sampling sites in the Pantanal floodplain (triangles) and in the neighbouring Cerrado upland plateaus (black circles), and cities (grey circles) in Mato Grosso do Sul, Brazil.

40.35” S and 57° 1’ 29.44” W), Fazenda Santa Clara S and 56° 22’ 25.90” W), Fazenda Dona Benedita (20° 20’ (19° 27’ 44.10” S and 57° 4’ 30.39” W), and Fazenda 44.78” S and 56° 26’ 13.12” W), Fazenda São Cristóvão Sagrado (19° 25’ 56.30” S and 57° 1’ 40.81” W). In the (20° 20’ 16.93” S and 56° 22’ 55.48” W), Fazenda São sub-region of Pantanal do Paraguai there was one site: Vicente (20° 31’ 25.37” S and 56° 24’ 56.63” W), Fazenda Fazenda Corumbá (19° 0’ 35.36” S and 57° 39’ 17.08” W). Santa Tereza (21° 5’ 14.27” S and 56° 3’ 10.63” W), Fazenda Campo Verde (21º 24’ 48.23’’ S and 56º 46’ 2.1.3. Upland plateau sampling sites 32.12’’ W), Fazenda Harmonia (21° 7’ 39.31” S and 56° Samplings comprised 16 sites in the plateau (Figure 1). 45’ 42.04” W), Fazenda Rancho Branco (20° 41’ 17.62” S In the Maracaju uplands there were six sites: Fazenda Furnas and 56° 46’ 42.40” W), Bonito (21° 7’ 38.46” S and 56° D’água (20° 9’ 29.38” S and 55° 24’ 16.02” W), Distrito 29’ 13.68” W). In the Maciço do Urucum uplands there de Camisão (20° 17’ 11.28” S and 55° 23’ 2.07” W), was one site (19° 18’ 52.42” S and 57° 36’ 12.19” W). Distrito de Piraputanga (20° 16’ 38.03” S and 55° 18’ 18.54” W), Fazenda Vista Alegre (20° 5’ 55.13” S and 2.2. Samplings and analyses 54° 27’ 26.67” W), Município de Campo Grande (20° 27’ This study relies on the bat scientific collection 4.58” S and 54° 36’ 57.38” W), Fazenda Taboco (20° 3’ organised by Dr. Valdir Antônio Taddei at Universidade 36” S and 55° 36’ 20” W). In the Bodoquena uplands there Anhanguera – Uniderp, Campo Grande, MS, between 1994 were nine sites: Fazenda Campina Grande (20° 21’ 22.32” and 2006, with 4,239 bat specimens collected through

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 311-320 313 Alho, CJR. et al. different procedures, predominantly straightforward mist- Otherwise, the number of phyllostomid species in plateaus net surveys, and on the Projeto Morcegos do Pantanal (n = 27) was slightly higher than in the floodplain (n = 23), databank at UFMS, Campo Grande, MS, with 4,798 bat contributing to the increased number of exclusively entries through mist-net captures between 1998 and 2007. frugivorous species in the plateaus (Figure 3). Although Surveys covered different hydrological seasons of the phyllostomids were richer in plateaus, the subfamily Pantanal and its surroundings in different habitats, near Phyllostominae presented more species in the floodplain; and fruiting trees, bat shelters, or forest canopies. Total capture it included all the insectivorous bats among phyllostomid effort was about 290,000 h.m2 (time in which nets were species. Therefore, insectivory appears to be a trait which kept open multiplied by the area of the nets), distributed favours the occurrence of bat species in the floodplain. throughout 376 nights, with four to 12 nets of variable sizes Indeed, even the frugivorous phyllostomids feed on open per night. Biometrical data were obtained and voucher insects proportionally more in the Pantanal floodplain specimens were prepared for identification, which followed than in its bordering plateaus or elsewhere (Munin, 2008; the criteria established by Vizotto and Taddei (1973), Teixeira et al., 2009). Diets toward insectivory might be Taddei (1983), Anderson (1997), Lopez-González et al. partially explained because insects are available throughout (2001), Gregorin and Taddei (2002), Vicente et al. (2005), the year, and massively during several months, whereas and Reis et al. (2006, 2007). bat fruit sources are markedly seasonal and poor in the Pantanal floodplain (Munin, 2008; Teixeira et al., 2009). 3. Results and Discussion Artibeus planirostris (n = 3,101 individuals) was by far the most dominant bat species throughout the entire focal 3.1. Bat fauna in south Pantanal and region (Figure 4), showing one order of magnitude more surrounding uplands captures than the next nine highly common species – Myotis nigricans (n = 762), Molossus molossus (n = 692), Noctilio In all 35 sites 9,037 individuals belonging to 56 species, albiventris (n = 681), Platyrrhinus lineatus (n = 633), 36 genera and six families were recorded (Table 1). This Sturnira lilium (n = 461), Carollia perspicillata (n = 451), number of species represents 34% of the whole richness Glossophaga soricina (n = 436), Artibeus lituratus (n = 320), of bats in Brazil, including the Amazon, annotated by and Desmodus rotundus (n = 281). Such strong dominance Reis et al. (2006, 2007); it reaches 62% of the total of A. planirostris has been also reported in other local richness reported for the entire Upper Paraguay River Basin surveys in the Pantanal floodplain and in its neighbouring (n = 90 bat species), including the northern area in Mato upland regions (Camargo, 2003; Camargo et al., 2009; Grosso, Brazil, and the Bolivian and Paraguayan areas Cunha et al., 2009; Teixeira et al., 2009). Although the (Tomas et al., 2009). In the floodplain sites, 6,292 individuals dominance by A. planirostris occurred in both regions, of 46 species were captured, a number which reaches 64% of in the Pantanal floodplain there were three insectivorous the bat species already registered in the whole Pantanal non‑phyllostomid species (Myotis nigricans, Noctilio floodplain (Tomas et al., 2009; Alho et al., 2003); in the albiventris, and Molossus molossus) among the most upland sites surrounding the Pantanal 2,745 individuals common bats, contrasting with the upland plateaus where of 44 species were recorded, representing 65% of the bat the commonest species were all frugivorous phyllostomids species already reported to occur along the entire Pantanal (Figure 4). The frugivorous C. perspicillata was the second borders (Tomas et al., 2009). The large number of captures most abundant species in the uplands, but it was not one and the cumulative curve of species captured (Figure 2), of the top ten species in the floodplain (Figure 4). Thus, throughout a relatively long period of time dedicated to the relative abundance of insectivorous bats appears to be survey (1994-2007), indicate that overall species richness higher in the floodplain than in the uplands, probably for the was well sampled and that this is a reliable representation same reasons which explain the exceptionally high richness of bat diversity in the focal region. In addition, five of insectivores as discussed above. Calculated values for species found here – Diphylla ecaudata, Mimon bennettii, the Shannon index of diversity were similar between the Trachops cirrhosus, Uroderma magnirostrum, and Molossus Pantanal floodplain (H’ = 2.3) and its neighbouring uplands pretiosus – were still not reported for Mato Grosso do Sul (H’ = 2.5). Assembling all the 35 sampling sites, diversity (Cáceres et al., 2008), increasing to 66 the number of bat was found to be H’ = 2.5. These values are higher than species registered in this state. those (H’ = 1.5 to 1.8) found in short-term surveys in the The richest and most abundant families in our 35 study Bodoquena region (Camargo et al., 2009; Cunha et al., sites were Phyllostomidae (30 species and 6,228 individuals) 2009), and closer to values (H’ = 1.8 to 2.3) found for and Molossidae (12 species and 1,071 individuals) (Table 1), different areas in the Atlantic forest in southeastern Brazil corresponding to 34% and 46% of the Brazilian species (Pedro and Taddei, 1997; Esbérard, 2003). in these two families respectively (Gregorin and Taddei, In pockets of cerrado habitats the most abundant species 2002; Reis et al., 2006, 2007). Richness of molossid bats are Artibeus planirostris (n = 431), Noctilio albiventris (all insectivorous) in the floodplain (n = 11) was almost (n = 381) and Molossus molossus (n = 362). In fragments twice that in the upland plateaus (n = 6), largely contributing of semi-deciduous and deciduous forest on plateaus on to the high number of insectivorous species exclusively the outskirts of the Pantanal the common species are: found in the floodplain rather than in plateaus (Figure 3). Myotis nigricans (n = 489), Noctilio albiventris (n = 168)

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Table 1. Number of surveyed individuals from 1995 to 2007 and feeding niche of 56 bat species in the Pantanal floodplain and its surrounding upland plateaus, Mato Grosso do Sul, Brazil. Number of individuals Family / Species Feeding niche Flood plain Plateau ∑ Phyllostomidae 3856 2372 6228 Artibeus planirostris (Spix, 1823) 2335 766 3101 Frugivore Platyrrhinus lineatus (E. Geoffroy, 1810) 382 251 633 Frugivore Sturnira lilium (E.Geoffroy, 1810) 199 262 461 Frugivore Carollia perspicillata (Linnaeus, 1758) 87 364 451 Frugivore Glossophaga soricina (Pallas, 1766) 225 211 436 Nectarivore Artibeus lituratus (Olfers, 1818) 177 143 320 Frugivore Desmodus rotundus (E. Geoffroy, 1810) 190 91 281 Sanguivore Anoura geoffroyi Gray, 1838 0 124 124 Nectarivore Lophostoma silvicolum d’Orbigny, 1836 84 13 97 Insectivore Phyllostomus hastatus (Pallas, 1767) 59 30 89 Frugivore Anoura caudifer (E. Geoffroy, 1818) 1 57 58 Nectarivore Phyllostomus discolor Wagner, 1843 39 7 46 Frugivore Chrotopterus auritus (Peters, 1856) 21 12 33 Carnivore Platyrrhinus helleri (Peters, 1866) 8 10 18 Frugivore Diaemus youngi (Jentink, 1893) 16 0 16 Sanguivore Lophostoma brasiliense Peters, 1866 9 2 11 Insectivore Mimon bennettii (Gray, 1838) 7 4 11 Insectivore Vampyressa pusilla (Wagner, 1843) 2 5 7 Frugivore Chiroderma villosum Peters, 1860 5 1 6 Frugivore Chiroderma doriae Thomas, 1891 2 3 5 Frugivore Mimon crenulatum (E. Geoffroy, 1810) 5 0 5 Insectivore Tonatia bidens (Spix, 1823) 1 4 5 Insectivore Micronycteris minuta (Gervais, 1856) 1 3 4 Insectivore Phylloderma stenops Peters, 1865 0 3 3 Frugivore Uroderma magnirostrum Davis, 1868 0 2 2 Frugivore Diphylla ecaudata Spix, 1823 0 1 1 Sanguivore Macrophyllum macrophyllum Schinz, 1821 0 1 1 Insectivore Pygoderma bilabiatum (Wagner, 1843) 0 1 1 Frugivore Trachops cirrhosus (Spix, 1823) 0 1 1 Carnivore Vampyrodes caraccioli (Thomas, 1889) 1 0 1 Frugivore Molossidae 833 238 1071 Molossus molossus (Pallas, 1766) 602 90 692 Insectivore Molossus rufus E.Geoffroy Saint-Hilaire, 1805 4 84 88 Insectivore Molossops temminckii (Burmeister, 1854) 50 21 71 Insectivore Cynomops abrasus (Temminck, 1827) 42 0 42 Insectivore Eumops auripendulus (Shaw, 1800) 34 6 40 Insectivore Molossus pretiosus Miller, 1902 39 0 39 Insectivore Nyctinomops macrotis (Gray, 1840) 0 28 28 Insectivore Promops centralis Thomas, 1915 26 0 26 Insectivore Cynomops planirostris (Peters, 1865) 21 0 21 Insectivore Eumops glaucinus (Wagner, 1843) 11 0 11 Insectivore Nyctinomops laticaudatus (E.Geoffroy Saint-Hilaire, 1805 1 9 10 Insectivore Promops nasutus (Spix, 1823) 3 0 3 Insectivore

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Table 1. Continued...

Number of individuals Family / Species Feeding niche Flood plain Plateau ∑ Vespertilionidae 895 92 987 Myotis nigricans (Schinz, 1821) 712 50 762 Insectivore Myotis albescens (E. Geoffroy, 1906) 109 7 116 Insectivore Eptesicus furinalis (d’Orbigny and Gervais, 1847) 15 21 36 Insectivore Lasiurus ega (Gervais, 1856) 22 1 23 Insectivore Myotis riparius Handley, 1960 15 4 19 Insectivore Myotis simus (Thomas, 1901) 18 0 18 Insectivore Lasiurus blossevillii (Lesson and Garnot, 1826) 0 7 7 Insectivore Eptesicus brasiliensis (Desmarest, 1819) 3 1 4 Insectivore Lasiurus cinereus (Beauvois, 1796) 1 1 2 Insectivore Noctilionidae 690 41 731 Noctilio albiventris Desmarest, 1818 641 40 681 Insectivore Noctilio leporinus (Linnaeus, 1758) 49 1 50 Piscivore Emballonuridae 18 0 18 Rynchonycteris naso (Wied-Neuwied, 1820) 13 0 13 Insectivore Peropteryx macrotis (Wagner, 1843) 5 0 5 Insectivore Mormoopidae 0 2 2 Pteronotus parnellii (Gray, 1843) 0 2 2 Insectivore ∑ 6292 2745 9037

Figure 3. Richness of bats according to feeding niche, based on 9,037 individuals examined belonging to 56 species, in the Pantanal fl oodplain and in its neighbouring upland Figure 2. Rarefaction curves for bats sampled in 19 sites in plateaus, Mato Grosso do Sul, Brazil. Light grey bars the Pantanal fl oodplain (a), and in 16 sites in the surrounding indicate species exclusive to the fl oodplain, grey bars upland plateaus (b), in Mato Grosso do Sul, Brazil. The species only found in plateau, and dark grey bars those upper curve refers to all these 35 sites assembled (c). occurring in both fl oodplain and plateau. and Molossus molossus (n = 155). In disturbed areas, habitats: Cerrado, disturbed habitats and semi-deciduous near the houses of cattle ranchers, the common species forest of plateaus. On the other hand, 24 rare species are: Carollia perspicillata (n = 129), Molossus molossus were detected, such as Chiroderma doriae, Chrotopterus (n = 125) and Artibeus planirostris (n = 97). Figure 5 shows auritus, and Artibeus lituratus (Table 1). Chiroderma the distribution of the species within three major kinds of doriae is a species which requires habitat integrity and so

316 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 311-320 Bat species richness in the Pantanal

Figure 4. Rank abundance distribution of 56 species of bats in a) the Pantanal floodplain and b) its surrounding upland plateaus in Mato Grosso do Sul, Brazil. Asterisks indicate species which were recorded in both the floodplain and uplands.

is sensitive to disturbance. Some authors (Bergallo et al., that the most caught family was Phyllostomidae, represented 2000) consider this species as threatened by extinction, but by Glossophaga soricina and Artibeus lituratus; and some it is not listed in the “Livro Vermelho da Fauna Brasileira rare species such as Lophostoma brasiliense, Lonchophylla Ameaçada de Extinção [The Red Book of Brazilian Fauna mordax and Lionycteris spurrelli (Bordignon, 2006). under Threat of Extinction]”, published by the Ministry To analyse possible grouping of species or assemblages for the Environment (Ministério do Meio Ambiente) in in the three major habitats, we performed a non-metric 2008. No species found in our survey for the Pantanal is multi-dimensional scaling analysis taking the frequencies officially listed as threatened. Chrotopterus auritus is a of species distribution, and found that the grouping large carnivore/insectivore, preying on small mammals, composed of Myotis albescens, Molossops temminckii, birds and insects, which is very sensitive to environmental Sturnira lilium, Phyllostomus hastatus, Desmodus rotundus, disturbance, requiring good forest habitats and shelter in Glossophaga soricina, Carollia perspicillata, Platyrrhinus caves. Artibeus lituratus was recorded at only 1.5% in our lineatus, Molossus molossus, Artibeus planirostris and study, but it is a good coloniser of disturbed habitat, besides Noctilio albiventris occurs in the three major habitats: living in low densities. The survey conducted in the region cerrado, semi-deciduous forest and disturbed habitats of Aporé-Sucuriú, northern Mato Grosso do Sul, revealed (with 82% of similarity).

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in abundance, whereas the abundance of frugivorous stenodermatines and nectarivorous glossophagines decreases (C. Santos, unpublished data). Our data show a high number of Phyllostomidae, which may represent a good indicator for low levels of habitat disturbance (Pedro at al., 1995; Pedro, 1998; Medellín et al., 2000). This family is well diversified in number of species and in feeding habits. The high number of frugivore species in the family implies that the habitats support a high number of fruit-bearing trees (see Pott and Pott, 1994). In addition, the high primary production favours an increased abundance of arthropods, which supports the guild of insectivore bats. The abundance of frugivore species reflects the importance of this guild for the Pantanal bat assemblages. In addition, bats play an important role in regulating the Pantanal ecosystem as seed Figure 5. Distribution of the bat species in three major dispersers, pollinators and regulators of insect populations habitats in Mato Grosso do Sul, Brazil. SAV: savanna (Gonçalves et al., 2007; Munin, 2008; Teixeira et al., 2009). or Cerrado; AA: disturbed areas near ranches and other human occupation; and ATE: the ecotone zone between Given that some bat species or bat assemblages require the floodplain and the upland “planalto”, covered by pristine habitat conditions while others are opportunistic, semi-deciduous forest. taking advantage of some disturbance, the group should be more studied as an indicator of levels of change in the natural environment. Drastic human alteration in natural habitats 3.2. Bat species as bio-indicator may result in simplifying bat diversity and assemblage, The Pantanal is undoubtedly an important domain since those species which require more specific items in and therefore deserves comprehensive ecosystem studies. feeding strategy tend to disappear, while those with a wide Our present information on bat species richness and spectrum of feeding habits, such as insectivore-omnivore assemblages, considering such abundant sampling data, and frugivore-omnivore, are generally less affected by contributes to making a more general interpretation of environmental changes. species magnitude for conservation purposes. Bat species, Effects of forest fragmentation on frugivore and for example, can serve as indicators for habitat quality. nectarivore species have been pointed out in French Natural habitats of the Pantanal have been disrupted by Guiana (Cossons, 1999). The role of frugivorous bats has non-sustainable practices of socio-economic development, been emphasised in tropical forest succession (Muscarella mainly by conversion of natural vegetation to pastures for and Flemming, 2007). Overall, Phyllostomid bats have cattle ranching and agriculture (Alho, 2008). Farms have been identified as indicators of habitat disruption in the Neotropics (Fenton et al., 1992). Work conducted in been established in the floodplain and in its surrounding forest habitats of Paraguay has shown that abundance was uplands, where much of the natural vegetation has been highest for Artibeus lituratus in deforested landscapes and converted to soybean plantations or to other human for Chrotopterus auritus in forested habitats; in contrast, activities. Studies concluded that 17% of the Pantanal has Artibeus fimbriatus, Carollia perspicillata, Glossophaga been deforested through the use of fire (mainly cerrado soricina, Platyrrhinus lineatus, Pygoderma bilabiatum, and patches or “capões de cerrado”), with an annual rate of Sturnira lilium attained highest abundance in moderately deforestation of 2.3%; and 63% of the natural vegetation fragmented forest landscapes. Forest cover, patch size, and cover of the surrounding plateaus in the Planalto (savanna patch density frequently were associated with abundance woodland and semi-deciduous forests) has been destroyed of species (Gorresen and Willig, 2004). (Harris et al., 2005). Deforestation between1976 and 2008 Therefore, our data indicate that bat species richness in the Pantanal floodplain increased 26.5 times (12.14%), and assemblages in the Pantanal and its surrounding compared to 40.97% of deforestation within the Upper habitats are still well preserved, and it is hoped that these Paraguay basin (Silva et al., 2010). findings may be useful for constructive lines of biodiversity In pastures continuously used for cattle ranching, the conservation and management in this important wetland dominance of A. planirostris in the bat assemblages is ecosystem. higher than in areas used intermittently by cattle (C. Santos, unpublished data), indicating that cattle ranching may cause Acknowledgements – This study was partially supported a reduction in bat diversity. In addition, fire events seem by the Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul to promote changes in bat species composition. Artibeus (FUNDECT) grants to Dr. Cleber Alho (Termo de Outorga planirostris has been found to be the most abundant bat in n.º 0133/06), to E. Fischer (Termos de Outorga n.º 131/04, both burned and unburned sites in the floodplain; however, 079/06, and 073/08), and a doctoral grant to C. Santos (Process after fire, the insectivorous phyllostomine bats increase n.º 41/100.271/2006); additional funds and field work support

318 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 311-320 Bat species richness in the Pantanal were provided by Earthwatch Institute, Fundação O Boticário COSSONS, JF., PONS, JM. and MASSON, B., 1999. Effects of de Proteção à Natureza, Conservation International, Wildlife forest fragmentation on frugivorous and nectarivorous bats in French Conservation Society, and Fundação Neotrópica do Brasil. Guiana. Journal of Tropical Ecology, vol. 15, no. 4, p. 515-534. Some data of this paper are part of the Master’s dissertation CUNHA, NL., FISCHER, E., CARVALHO, LFAC. and SANTOS, of Larissa F. Oliveira‑Pissini, working under the academic CF., 2009. Bats of Buraco das Araras natural reserve, southwestern and scientific advice of Professor Cleber Alho at Uniderp. We Brazil. Biota Neotropica, vol. 9, no. 4. Available from: . Master’s program of Uniderp – for his support. We would like to emphasise the enormous value of the bat scientific collection DROBNER, U., BIBBY J., SMITH, B. and WILSON, JB., 1998. constructed by Dr. Valdir Antonio Taddei, and in his honour – The relation between community biomass and evenness: what in memoriam – we dedicate this work. Celina Alho and Susan does theory predict, and can these predictions be tested. Oikos, Casement reviewed the manuscript. vol. 82, p. 295-302. ESBÉRARD, CEL., 2003. Diversidade de morcegos em uma área References de Mata Atlântica regenerada no sudeste do Brasil (Mammalia: Chiroptera). Revista Brasileira de Zoociências, vol. 5, p. 189-204. AGUIRRE, LF., 2002. Structure of a Neotropical savanna bat community. Journal of Mammalogy, vol. 83, no. 3, p. 775-784. FALCÃO, FC., REBÊLO, VF. and TALAMONI, SA., 2003. Structure of a bat assemblage (Mammalia, Chiroptera) in Serra ALHO, CJR., 2005. The Pantanal. In FRASER, LH. and KEDDY, do Caraça Reserve, South-east Brazil. Revista Brasileira de PA., Org. The World’s Largest Wetlands – Ecology and Conservation. Zoologia, vol. 20, no. 2, p. 347-350. New York, USA: Cambridge University Press, p. 203-271. FENTON, MB., ACHARYAL, L., AUDET, D., HICKEY, MBC., -, 2008. Biodiversity of the Pantanal: response to seasonal flooding MERRIMAN, C., OBRIST, MK., SYME, DM. and ADKINS, regime ant to environmental degradation. Brazilian Journal of B., 1992. Phyllostomid bats (Chiroptera:Phyllostomidae) as Biology, vol. 68, no. 4, p. 957-966. Suppl. indicators of habitat disruption in the Neotropics. Biotropica, vol. 24, p. 440-446. ALHO, CJR., STRUSSMANN, C., VOLPE, M., SONODA, F., MARQUES, AAB., SCHNEIDER, M., SANTOS JUNIOR, TS. and GONÇALVES, F., MUNIN, R., COSTA, P. and FISCHER, MARQUES, SR., 2003. Conservação da biodiversidade da Bacia E., 2007. Feeding habits of Noctilio albiventris (Noctilionidae) do Alto Paraguai. Campo Grande, MS: Editora UNIDERP. 466 p. bats in the Pantanal, Brazil. Acta Chiropterologica, vol. 9, no. 2, p. 535-546. ANDERSON, S., 1997. Mammals of Bolivia: taxonomy and distribution. Bulletin of the American Museum of Natural History, GORRESEN, PM. and WILLIG, MR., 2004. Landscape responses no. 231, 652 p. of bats to habitat fragmentation in Atlantic Forest of Paraguay. Journal of Mammalogy, vol. 85, no. 4, p. 688-697. ARAÚJO, AC. and SAZIMA, M., 2003. The assemblage of flowers visited by hummingbirds in the “capões” of southern GREGORIN, R. and TADDEI, VA., 2002. Chave artificial para a Pantanal, Mato Grosso do Sul, Brazil. Flora, vol. 198, p. 427-435. identificação de molossídeos brasileiros (Mammalia, Chiroptera). Mastozologia Neotropical, vol. 1, no. 9, p. 13-32. BERGALLO, HG., GEISE, L., BONVICINO, CR., CERQUEIRA, R., D’ANDREA, PS., ESBÉRARD, CE., FERNANDEZ, FAS., HARRIS, MB., ARCANGELO, C., PINTO, ECT., CAMARGO, GRELLE, CE., PERACCHI, A., SICILLIANO, S. and VAZ, SM., G., RAMOS-NETO, MB. and SILVA, SM., 2005. Estimativas 2000. Mamíferos. In BERGALLO, MV., ROCHA, CFD., ALVES, de perda da área natural da Bacia do Alto Paraguai e Pantanal MAS., SLUYS, MV., Org. A fauna ameaçada de extinção do Brasileiro. Campo Grande, MS: Conservation International. Estado do Rio de Janeiro. Rio de Janeiro, Ed. UERJ. p. 125-135. Unpublished Technical Report. BORDIGNON, MO., 2006. Diversidade de morcegos (Mammalia, KEDDY, PA., FRASER, LH., SOLOMESHCH, AI., JUNK, WJ., Chiroptera) do Complexo Aporé-Sucuriú, Mato Grosso do Sul, CAMPBEL, DR., ARROYO, MTK. and ALHO, CJR., 2009. Brasil. Revista Brasileira de Zoologia, vol. 23, no. 4, p. 1002-1009. Wet and wonderful: the word’s largest wetlands are conservation priorities. BioScience, vol. 59, no. 1, p. 39-51. CÁCERES, NC., CARMIGNOTTO, AP., FISCHER, E. and SANTOS, CF., 2008. Mammals from Mato Grosso do Sul, Brazil. LEITE, A., MENEGHELLI, M. and TADDEI, VA., 2000. Check List, vol. 4, no. 3, p. 321-335. Morcegos do Pantanal do Estado do Mato Grosso do Sul. In Anais do II Encontro de Pesquisa e Iniciação Científica da UNIDERP. CAMARGO, G. and FISCHER, E., 2005. Primeiro registro do Campo Grande. p. 129-131. morcego Mimon crenulatum (Phyllostomidae) no Pantanal, sudoeste do Brasil. Biota Neotropica, vol. 5, no. 1. Available from: . de espécies. Ensaios e Ciência, vol. 2, no. 2, p. 167-174. CAMARGO, G., 2003. Riqueza e diversidade de morcegos no LONGO, JM., FISCHER, E., CAMARGO, G. and SANTOS, Pantanal do Miranda-Abobral, Mato Grosso do Sul. Campo CF., 2007. Occurrence of Vampyressa pusilla Chiroptera, Grande: Universidade Federal de Mato Grosso do Sul. 51 p. Phyllostomidae) in Southern Pantanal. Biota Neotropica, vol. 7, Dissertação de mestrado em ecologia e conservação. no. 3. Available from: . CAMARGO, G., FISCHER, E., GONÇALVES, F., FERNANDES, G. and FERREIRA, S., 2009. Morcegos do Parque Nacional da LÓPEZ-GONZÁLEZ, C., PRESLEY, SJ., OWEN, RD. and WILLIG, Serra da Bodoquena, Mato Grosso do Sul, Brasil. Chiroptera MR., 2001. Taxonomic status of Myotis (Chiroptera:Vespertilionidae) Neotropical, vol. 15, no. 1, p. 417-424. in Paraguay. Journal of Mammalogy, vol. 1, no. 82, p. 138-160.

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 311-320 319 Alho, CJR. et al.

MARINHO-FILHO, J. and SAZIMA, I., 1998. Brazilian bats do Pantanal através de levantamento aéreo. Revista Brasileira de and conservation biology; a First Survey. In KUNZ, TH. and Botânica, vol. 23, no. 2, p. 143-152. RACEY, PA., Ed. Bat, biology and conservation. Washington, STEVENS, RD. and WILLIG, MR., 2002. Geographical ecology D.C.: Smithsonian Institution Press. p. 282-294. at the community level: perspectives on the diversity of New MEDELLÍN, RA., EQUÍHUA, M. and AMIN, MA., 2000. Bat World bats. Ecology, vol. 83, no. 2, p. 543-560. diversity and abundance as indicators of disturbance in Neotropical TADDEI, VA., 1983. Morcegos – Algumas considerações rainforests. Conservation Biologi, vol. 14, p. 1666-1675. sistemáticas e biológicas. Campinas: Coordenadoria de Assistência MUNIN, RL., 2008. Utilização e sobreposição de itens alimentares Técnica Integral. 31 p. por morcegos filostomídeos no Pantanal da Nhecolândia, Mato TADDEI, VA., LEITE, AP., VICENTE, EC., SOUZA, HA. Grosso do Sul. Campo Grande: Universidade Federal de Mato and MENEGHELLI, M., 2000. Morcegos da Estância Caiman, Grosso do Sul. 41 p. Dissertação de mestrado em ecologia e Município de Miranda, Estado do Mato Grosso do Sul. In Anais conservação. do II Encontro de Pesquisa de Iniciação Científica da UNIDERP. Campo Grande. p. 128-129. MUSCARELLA, R. and FLEMMING, TH., 2007. The role of frugivorous bats in tropical forest succession. Biological Reviews, TADDEI, VA., PULCHÉRIO, AL. and MENEGHELLI, M., vol. 82, p. 573-590. 2001. Morcegos de áreas antropizadas da Estância Caiman, Município de Miranda, Estado do Mato Grosso do Sul. In Anais PATTERSON, BD., WILLIG, MR. and STEVENS, RD., 2001. do XII Encontro de Biólogos do CRB-1. Campo Grande: UFMS. Tropic strategies, niche partitioning, and patterns of ecological vol. 1, p. 87. organization. In KUNZ, TH. and FENTON, MB., Ed. Bat ecology. Chicago, Illinois, USA: University of Chicago Press. TADDEI, VA., VICENTE, EC., PULCHÉRIO-LEITE, A. and MERCANTE, MA., 2003. Morcegos (CHIROPTERA: PEDRO, WA. and TADDEI, VA., 1997. Taxonomic assemblage of MAMMALIA) da região do Instituto de Pesquisa do Pantanal, bats from Panga Reserve, southeastern Brazil: abundance patterns sub-região do Rio Negro, MS, Brasil. Ensaios e Ciência, vol. 1, and trophic relations in the Phyllostomidae (Chiroptera). Boletim no. 1, p. 681-687. Ed. especial. do Museu Biológico Mello Leitão, vol. 6, p. 3-21. TEIXEIRA, RC., CORREA, CE. and FISCHER, E., 2009. PEDRO, WA., 1998. Diversidade de morcegos em habitas Frugivory by Artibeus jamaicensis (Phyllostomidae) bats in the florestais fragmentos do Brasil (Chiroptera; Mammalia). São Pantanal, Brazil. Studies on Neotropical Fauna and Environment Carlos: Universidade Federal de São Carlos. 128 p. Tese de vol. 44, no. 1, p. 7-15. doutorado em ecologia e recursos naturais. TOMAS, WM., CÁCERES, NC., NUNES, AP., FISCHER, E., PEDRO, WA., GERALDES, MP., LOPES, GG. and ALHO, CJR., MOURÃO, GM. and CAMPOS, Z., 2009. Mammals in the Pantanal 1995. Fragmentação de habitat e a estrutura de uma taxocenose wetland, Brazil. In: JUNK, WJ., SILVA, CJ., CUNHA, CN. and de morcegos em São Paulo (Brasil). Chiroptera Neotropical, WANTZEN, KM., Org. The Pantanal: ecology, biodiversity and vol. 1, no. 1, p. 4-6. sustainable management of a large neotropical seasonal wetland. Sofia: Pensoft Publishers. p. 127-141. POTT, A. and POTT, VJ., 1994. Plantas do Pantanal. Corumbá: EMBRAPA/CPAP. 320 p. VICENTE, EC., TADDEI, VA. and JIM, J., 2005.Características morfológicas externas distintivas de Myotis albescens, M. nigricans, REIS, NR., PERACCHI, A., PEDRO, WA. and LIMA, IP., Ed., M. simus e M. riparius (Chiroptera;Vespertilionidae). Ensaios e 2007. Morcegos do Brasil. Londrina. 253 p. Ciência, vol. 9, no. 2, p. 293-304. -, 2006. Mamíferos do Brasil. Londrina. 437 p. VIZOTTO, LD. and TADDEI, VA., 1973. Chave para determinação de quirópteros brasileiros. Revista da Faculdade de Ciências e Letras ROHDE, K., 1992. Latitudinal gradients in species diversity: the de São José do Rio Preto – Boletim de Ciências, no. 1, p. 1-72. search for the primary cause. Oikos, vol. 65, p. 514-527. WILLIG, MR., 2000. Latitude, common trends within. In LEVIN, SCARIOT, A., SOUSA-SILVA, JC., FELFILI, JM., Ed., 2005. SA., Ed. Encyclopedia of biodiversity. Burlington, Massachusetts, Cerrado: ecologia, biodiversidade e conservação. Brasília: USA: Academic Press. vol. 3, p. 701-714. Ministério do Meio Ambiente. 439 p. WILLIG, MR., PRESLEY, SJ., OWEN, RD. and LÓPES- SILVA, JSV. and ABDON, MM., 1998. Delimitação do Pantanal GONZÁLES, C., 2000. Composition and Structure of Bat brasileiro e suas sub-regiões. Pesquisa Agropecuária Brasileira, Assemblages in Paraguay: A Subtropical-Temperate Interface. vol. 33, no. especial, p. 1703-1711. Journal of Mammalogy, vol. 81, no. 2, p. 386-401. SILVA, JSV., ABDON, MM., MORAES, JA., 2010. Desmatamento WILSEY, BJ. and POTVIN, C., 2000. Biodiversity and ecosystem na bacia do Alto Paraguai no Brasil. In Anais 3º Simpósio de functioning: importance of species evenness in an old field. Geotecnologias no Pantanal. Cáceres, MT, 16-20 de outubro Ecology, vol. 81, p. 887-892. 2010. Embrapa Informática Agropecuária/INPE, p. 459-467. ZORTÉA, M. and ALHO, CJR., 2008. Bat diversity of a Cerrado SILVA, MP., MAURO, R., MOURÃO, G. and COUTINHO, habitat in central Brazil. Biodiversity and Conservation, vol. 17, M., 2000. Distribuição e quantificação de classes de vegetação no. 4, p. 791-805.

320 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 311-320 Introduced species in the Pantanal: implications for conservation Alho, CJR.a*, Mamede, S.b*, Bitencourt, K.c* and Benites, M.d* aPrograma de Pós-graduação em Meio Ambiente e Desenvolvimento Regional, Universidade Anhanguera – Uniderp, CEP 79070-900, Campo Grande, MS, Brazil bInstituto Physis Cultura e Ambiente, Rua Dona Ana, 11b, Vila Mariana, CEP 04111-070, São Paulo, SP, Brazil cUniversidade Anhanguera – Uniderp, CEP 79070-900, Campo Grande, MS, Brazil dDepartamento de Zootecnia, Universidade Estadual de Mato Grosso do Sul – UEMS, Unidade Universitária de Aquidauana, Rod. Aquidauana/Cera, Km 12, CEP 79200-000, Aquidauana, MS, Brazil *e-mail: [email protected], [email protected], [email protected], [email protected] Received October 14, 2010 – Accepted December 13, 2010 – Distributed April 30, 2011

Abstract Land use and human occupation within the natural habitats of the Pantanal have facilitated introduction of invasive species of plants and animals, including domestic species. Exotic species threaten regional biodiversity because they modify ecological community structure, alter natural habitats and affect local biodiversity. An international organisation, the International Union for Conservation of Nature (IUCN), and the Brazilian government, identify invasive species as the third most important threat to biodiversity, following habitat loss and direct effect on species. In addition, exotic species carry pathogens or may function as vectors or reservoirs for diseases that affect regional biota. Keywords: biodiversity, exotic species, invasive species, introduced species, Pantanal.

Espécies introduzidas no Pantanal: implicações para conservação

Resumo O uso da terra e a ocupação humana nos hábitats naturais do Pantanal têm facilitado a introdução de espécies invasivas de plantas e animais, incluindo espécies domésticas. As espécies exóticas ameaçam a biodiversidade regional porque modificam a estrutura das comunidades ecológicas, alteram hábitats e afetam a biodiversidade. A organização internacional União Internacional para a Conservação da Natureza (IUCN) e o Governo brasileiro identificam as espécies invasoras como a terceira maior ameaça para a biodiversidade, seguida da perda de hábitat e do efeito direto sobre espécies. Além disso, espécies exóticas são portadoras de patógenos ou podem funcionar como vetores ou reservatórios de doenças que afetam a biota. Palavras-chave: biodiversidade, espécies exóticas, espécies invasivas, espécies introduzidas, Pantanal.

1. Introduction Following human occupation, there have been that each country that is party to the Convention has to introductions of exotic plants and animals, in a deliberate make efforts to control or eradicate exotic species. The or accidental manner, with consequent alterations of the MMA publication on the subject mentions 176 exotic natural ecological communities within the Pantanal. species occurring within terrestrial environments in Brazil, An introduced species is one which occurs outside its including 68 invasive animal species and 108 species of geographical distributional range, being an alien, exotic, flora. Additionally, 49 invasive species were identified non-indigenous, invasive or non-native species. These for aquatic ecosystems of Brazilian continental waters, species threaten biodiversity because they modify the including one microorganism, one crustacean, six aquatic community structure, changing the habitat and displacing macrophytes, four mollusks and 37 species of fish. Exotic native species. species found within the productive fields (crops, ranches The Brazilian Ministry for the Environment (Ministério and farms) were 155 species, including bacteria, fungus, do Meio Ambiente - MMA) considers introduced species insects and other arthropods. the second greatest cause of species extinction, affecting A global population of 6 billion people and rapid means biodiversity (Coradin, 2006). The Convention on Biological of transport increase the spread of invasive species. For Diversity, signed by Brazil, in its Article 8 (h) establishes example, the vector for dengue in Brazil is the mosquito Aedes

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 321-325 321 Alho, CJR. et al. aegypti (Linnaeus, 1762), which came from , probably Mesosetum loliiforme (Hochst. ex Steud.) and Panicum from the Ethiopian region, brought with slave‑trafficking laxum Sw., covering the open fields and sandy soils of the ships in the 16th to 19th centuries. Another introduced floodplain. Other plant species forming homogeneous fields species is Aedes albopictus (Skuse, 1895), which came are present, such as the legume Desmodium barbatum (L.) to Brazil in 1986 and can be the vector for yellow fever Benth and the fura-bucho belonging to the genus Paspalum (Segura et al., 2003; Walker 2007). (Santos et al., 2006). Since these natural pasture fields The International Union for Conservation of Nature remain submerged during the wet season, cattle ranchers (IUCN) created the Invasive Species Specialist Group are introducing exotic grassland species on the higher (ISSG) as a global network of scientific and policy experts grounds of the Pantanal. Cultivated pastures have been to deal with introduced species. They indicate that invasive expanding rapidly in the floodplain to compete with the species are the third most severe threat to wild mammals ranchers located in the upper Cerrado plateaus surrounding after habitat loss and utilisation such as hunting for food; the Pantanal. Two exotic species dominate the pastures: invasive species are also the third most severe threat to birds; Brachiaria decumbens Stapf and Brachiaria humidicola the fourth cause of death among reptiles (after pollution (Rendle)Schweick. These two exotic species aggressively persecution and natural disasters); and the fifth most severe cover the ground and have been widely used to convert threat to Amphibians (following habitat loss, pollution, natural vegetation into cultivated pastures. diseases and fires). The IUCN maintains a database named Grasses are among the invasive species with a high Global Invasive Database (http://www.issg.org/database/ capacity to colonise woodland, such as denser areas of welcome/). Cerrado that is being converted into open fields. In the The introduction of species may be intentional or case of B. decumbens, its capacity to exclude native species involuntary, but it is always related to human action and has been pointed out (Matos and Pivello, 2009; Oliveira, always results in environmental disruption (Fine, 2002). 2004). On the plateaus surrounding the Pantanal, grass The negative effects include predation, competition, species such as B. decubens and capim-gordura Melinis consequences of wild fire (since introduced species may minutiflora Beauv. are great challenges for control in recover better after a fire), and many other processes which protected areas. This is also the case of Emas National lead to displacement of native species and alteration of Park (Parque Nacional de Emas) in the state of Goiás, east natural ecological communities (Alho and Gonçalves, of the Pantanal. It has been shown that B. decumbens is 2005; Alho, 2005, 2008; McGeoch et al., 2010). the species that most benefits from wild fire, common in The aim of this review article is to evaluate the present the region during the dry season. role of invasive exotic species within the Pantanal habitats, There are some local plant species of the Pantanal which based on existing published knowledge, to discuss their take advantage of disturbed areas and grow aggressively, possible effects on ecological communities and to consider dominating and modifying natural habitats. Species locally the consequences of this threat on conservation objectives. known as assa-peixe (Vernonia scraba Pers. and Vernonia ferruginea Less.), can colonise areas along open routes or 2. Results and Discussion roads. Other species which benefit from altered habitats, proliferating abnormally, are Bromelia balansae Mez. The Pantanal and its surrounding upland plateau and Byrsonima intermedia A.Juss, B. orgignyana A. Juss have experienced the introduction of alien species and Licania parvifolia Huber. The bush locally known as such as the African grass Brachiaria (Griseb) spp., the pombeiros, belonging to the genus Combretum, can form feral hog Sus scrofa (Linnaeus, 1758), locally known homogeneous plots known as pombeiral after certain types as “porco monteiro”, and recently the golden mussel of disturbance and abnormal flooding. The same trend is Limnoperna fortunei (Dunker, 1857), locally known as observed with the proliferation of the cambará (Vochysia “mexilhão‑dourado”, accidentally brought from China. divergens Pohl.), forming homogeneous cambarazais; The Amazonian fish “tucunaré” Cichla cf. ocellaris Bloch and the dominance of lixeira (Curatella americana L.) & Schneider 1801, a voracious predator introduced in the forming lixeirais (Santos et al., 2006). Pantanal, has already impacted the regional fish community. 2.2. Livestock Herbivores like cattle and water buffalo can wreak great damage, since they require introduced pastures and exert Cattle-ranching is an important economic activity pressure on native plant species. within the Pantanal. The introduction of water buffalo The domestic animals introduced, with effects on natural (Bubalus bubalis Linnaeus, 1758) is relatively recent. It systems, include cattle, horses, dogs, cats, chickens and is estimated that there are more than 5000 head of buffalo many others, all from direct human action. Alien species in the region (Mourão et al., 2002). in the Pantanal have caused alterations in the life history In addition to the conversion of natural vegetation into of native plants as well as of wild animals. introduced cultivated pastures, the intensely herbivorous diet of cattle alters vegetation cover, modifying community 2.1. Introduced plants structure. The evidence of the effects of large domestic Natural pastures of the Pantanal are mainly formed herbivores, such as cattle and water buffalo, grazing on by species such as Axonopus purpusii (Mez) Chase, vegetation may be seen in recently protected areas where

322 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 321-325 Introduced species in the Pantanal cattle used to be established: the open areas immediately use between feral pigs and peccaries in the Pantanal were recover in structure and function. Herbaceous phytomass is found to be lower than expected (Desbiez et al. 2009). consumed under different grazing strategies by cattle and In fact, this study shows that niche overlap was highest water buffalo, which are distinguished by their effects on between the native species. Differences in morphology herbaceous productivity. There are direct effects on plant and behaviour indicate possible mechanisms of niche productivity and survival; besides constant loss of biomass partitioning between the species. to herbivores, grazing usually results in the introduction of 2.4. African bees exotic species. Large domestic herbivores affect vegetation, both directly by consuming a large portion of its biomass The African bee Apis mellifera scutellata (Lepeletier and also indirectly by being selective in preferred items, 1836) was introduced into Brazil in 1956 and has spread compacting the soil, foraging on woody vegetation throughout the country and others in the region. The so-called (browsing) and dispersing seed-propagating species, such ‘africanized bee’ or abelha africanizada is a hybrid of the as the acuri palm tree Attalea phalerata Mart. ex Spreng. European bee Appis mellifera mellifera Linnaeus, 1758. It has adapted very well to the environmental conditions 2.3. Feral pig of the biome and exhibits aggressive behaviour, attacking The feral pig, known in the Pantanal as porco-monteiro, humans and animals, such as horses, in the Pantanal. escaped from domestic herds and became wild. These 2.5. Introduced fishes animals form groups, then damaging crops, digging up large areas of native vegetation, particularly near the depressions The tucunaré is believed to have been introduced in the region in the 80’s. It is thought that the introduction occurred with temporary or permanent water known as baías, and in 1982, when a water reservoir for raising tucunaré broke, may transmit disease to wildlife. It has been estimated releasing the fishes into the Itiquira and Piquiri rivers, on the that there are nearly 10,000 groups of porco-monteiro in border of the states of Mato Grosso and Mato Grosso do Sul the Pantanal (Mourão et al., 2002). It is more abundant in (Ferraz de Lima, 1993). Surveys carried out indicate that the sub-region of Aquidauana and within the regions with tucunarés were confined to the Piquiri river basin between less flooding, such as Nhecolândia and Paiaguás. A study 1992 and 1994 (Nascimento et al., 2001). However, over carried out in the Pantanal of Rio Negro, between April the following years, the fish has been reported occurring 2003 and March 2004, showed that the porco-monteiro was in other river basins of the Pantanal, including in several the second most abundant mammal in the survey, second localities along the left bank of the Paraguay river, São only to capybara Hydrochoerus hydrochaeris Linnaeus, Lourenço River and Paraguay-Mirim River, (Marques 1766 (Mamede, 2004). Seasonally flooded habitats are and Resende, 2005). The tucunaré does not migrate for preferred by the animals, which particularly forage in reproduction and prefers clear and non-turbulent water. sites near temporary baías. This large fish is a voracious Amazonian carnivore The porco-monteiro has rapidly adapted to the preying upon native species, competing for food and space environmental conditions of the Pantanal, with with local species, disrupting ecological fish communities morpho‑physiological and behavioural characteristics in a cascading scale in the trophic food chain (Harris et al., that resemble its original wild ancestors more than the 2005). However, there are no regional studies on the real domestic pig. They are omnivorous and can occasionally role of tucunaré in the Pantanal aquatic habitats. prey upon young animals. They also take eggs and all kinds Another fish species recorded in the Pantanal is the of soil invertebrates and vertebrate species they are able Amazonian tambaqui (Colossoma macropomum Cuvier, to capture. Local residents hunt juveniles for food. Some 1816) whose biology resembles the natural history of the of the young males are captured, castrated and released local pacu (Piaractus mesopotamicus Holmberg, 1887), to be caught again, when older, for food. both feed largely on fallen fruits and seeds. Feral pigs probably occupy the same habitat requirements that local white-lipped peccary or queixada (Tayassu 2.6. Introduced mollusk peccary Link, 1795) and collared peccary cateto (Pecari The bivalve mollusk Limnoperna fortunei (Dunker, tajaco Linnaeus, 1758) do, particularly in terms of feeding 1857), known as mexilhão-dourado, was introduced into strategies (Sicuro and Oliveira, 2002). Niche partitioning the Paraná-Paraguay rivers and has reached the Pantanal. among sympatric populations of white-lipped peccary, It arrived in Argentina’s River Plate in 1991, brought by collared peccary, and feral hog was evaluated using an ships from China (Darrigan and Pastorino, 1995, 2003; ecomorphological approach: morphofunctional data suggest Oliveira et al., 2000). Ships arriving from Asia had that feral hogs have a powerful bite and are able to feed discharged ballast water containing the mussels or their on seeds of different degrees of resistance (Sicuro and larvae into the Plate. From this river, the molluscs reached Oliveira, 2002). This study indicates that with an optimised the Paraná-Paraguay rivers, giving them access to the vast lever system of head elevation, feral pigs are more efficient Pantanal wetland. than peccaries at rooting. In addition, feral hogs explore a It has been reported to occur in the Paraguay River wide range of habitats, which supports the view that the since 1998, up to the region of Bela Vista do Norte, near invasive species acts as a potential competitor of native the tributary of the Cuiabá River, in several lakes or baías peccaries. However, overlaps in food resources and habitat adjacent to the Paraguay River; and later on, in 2003, it

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 321-325 323 Alho, CJR. et al. was also reported in the Miranda river, near the region of By interacting with many species in a variety of ways, Passo do Lontra (Oliveira, 2003). introduced species affect, in an array of changes, the It also occurs at the bottom of a lake (Baía do ecological communities. Interactions among the species Tuiuiú ‑18º 49’ 18” S and 57º 39’ 13” W), near Corumbá are essential in the function of communities holding the city. In 1999 it was registered in the Paraguay River interacting species together and determine their specific (17º 38’ 04” S and 57º 41’ 45” W), near Forte Coimbra, roles. The most prominent processes are competition, encrusted on rocks. However, a study carried out by Oliveira predation, parasitism, herbivory, and mutualism. (2003) points out that the densities of mexilhão-dourado We need specific studies to characterise negative impacts in the Paraguay river (10,000 individuals/ m²) are lower qualitatively as well as quantitatively. With the present than the densities found in aquatic habitats in southern knowledge, all we can observe are the most immediate Brazil (100,000 individuals/ m²). and obvious effects on local biodiversity and natural Another introduced mollusk is the African snail habitats. Introduced species in the Pantanal obviously rely Achatina fulica Bowdich, 1822, which arrived in Brazil on predation, browsing, competition for food, nest sites, around 1980, brought to substitute the escargot Helix in addition to potential transmission of diseases. One of aspersa Müller, 1774 as a delicacy (Carvalho Jr. and these effects or the sum of them may alter community Nunes, 2009). Achatina fulica is partially an arboreal and structure and function and habitat quality; in this case, for herbivore generalist species and was introduced into the example, in terms of habitat loss by native species, due to Pantanal as bait brought by fishermen. This African mollusk environmental changes. is currently found throughout the Pantanal (Carvalho Jr. The negative impact of an exotic species on a population and Nunes, 2009; Instituto Horus, 2009; Teles et al., 1997). of native species of plants and animals is to reduce the The North-American frog Rana catesbeiana Shaw, population density of the vulnerable local species. In this 1802 = Lithobates catesbeianus (Shaw, 1802) was introduced case, the negative impact may cause a direct effect on into Brazil to be raised as a food source; it accidentally the local species (competition for food or nesting site, for escaped and is now found in several different regions. example) or adverse effects on habitat quality. There is no official record of this species in the Pantanal, When an ecological community of interacting animals and plants are disrupted, invasive species can take advantage but some people claim to have heard its call. of the changed conditions to establish themselves. In some 2.7. Dogs, cats, rats, mice and others habitats of the Pantanal introduced species become part Domestic or pest mammal species introduced by of the landscape, while others thrive at the expense of man into the Pantanal, including the domestic dog Canis native species. In many cases the invasive species exerts familiaris Linnaeus, 1758, cat Felis catus Linnaeus, 1775, additional stresses on the local and native species, with mouse Mus musculus (Linneaus, 1758) and black rat disruption to community structure and function. Since Rattus rattus (Linnaeus, 1758), are potential predators the invasive species does not have the natural predators of wildlife and infest ecological ecosystems, spreading from its original land to keep its numbers in check, it is diseases and causing habitat degradation. Cats are known able to spread throughout new habitats in the Pantanal. As to prey on birds’ nests and on lizards, amphibians and other soon as the invasive species of plant or animal becomes small animals. Dogs are trained to hunt wildlife. In some established, these invaders become hard to control. As protected areas feral dogs may impact biodiversity. The we have seen in the cases of the feral pig porco-monteiro effect of these alien invasive species may be viewed as the and the introduced Amazonian fish tucunaré they prey simple and direct effect of one given introduced species on or compete with native species. In terms of fauna, on any natural ecosystem. However, in a more complex introduced African grass species drastically modify the species composition of open habitats of the Pantanal. analysis, considering a greater number of variables that can There is no specific control programme in the Pantanal be identified and derived from invasive species, domestic to restore and prevent new invasions and keep established mammals and others can be examined simultaneously invasive species in check. Inside a broad conservation interacting among themselves as well as with the native programme, there is the need to restore, protect and preserve species. The result is generally the impoverishment of natural habitats, including research into invasive species local biodiversity. These species may also carry diseases in ecological communities and ecosystems, to keep these that affect wildlife and man: dogs, for example, harbour established invaders under control. the pathogen of leishmaniasis. Acknowledgements – We thank the organisers of this 2.8. Concluding remarks Volume and participants, especially Dr. José Tundisi From the introduced species reviewed here, the adverse (Executive Editorial Board of Brazilian Journal of effect of invasive species on biodiversity and natural Biology), Dr. Takako Matsumura‑Tunidsi (Editor in Chief of the Journal) and Prof. Elizabeth Brunini Sbardelini habitats of the Pantanal is evident. Some alterations in (University Anhanguera/Uniderp). We are grateful to Celina community structure and function have been rapid and Alho for assistance in preparing the manuscript, providing highly noticeable, while others are slow but ongoing; both helpful comments and organising its structure. Susan Casement trends, however, impact local biota. reviewed the language.

324 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 321-325 Introduced species in the Pantanal

References MARQUES, DKS. and RESENDE, EK., 2005. Distribuição do Tucunaré Cichla cf. monoculus (Osteichthyes, Ciclidae) no ALHO, CJR., 2005. The Pantanal. In FRASER, LH. and KEDDY, Pantanal. Corumbá: Embrapa Pantanal. Boletim de Pesquisa, no. 60. PA., Org. The World’s Largest Wetlands – Ecology and Conservation. MATOS, DMS. and PIVELLO, VR., 2009. O impacto das plantas New York, USA: Cambridge University Press. p. 203-271. invasoras nos recursos naturais de ambientes terrestres: alguns casos brasileiros. Ciência e Cultura (SBPC), vol. 61, p. 27-30. -, 2008. Biodiversity of the Pantanal: response to seasonal flooding regime and to environmental degradation. Revista Brasileira McGEOCH, MA., BUTCHART, SHM., SPEAR, D., MARAIS, E., de Biologia = Brazilian Journal of Biology, vol. 68, no. 4, KLEYNHANS, EJ., SYMES, A., CHANSON, J. and HOFFMANN, p. 957‑966. Suppl. M., 2010. Global indicators of biological invasion: species numbers, biodiversity impact and policy responses. Diversity ALHO, CJR. and GONÇALVES, HC., 2005. Biodiversidade do and Distributions, vol. 16, no. 95-108. Pantanal: ecologia e conservação. Ed. UNIDERP. 142 p. MOURÃO, G., COUTINHO, ME., MAURO, R., TOMÁS W. CARVALHO Jr., VCB. and NUNES JRS., 2009. Occurrence and and MAGNUSSON, W., 2002. Levantamentos aéreos de espécies distribution of the african snail “Achatina fulica” Bowdich, 1822, introduzidas no Pantanal: porcos ferais (porco monteiro), gado at the county of casa grande, state of mato grosso. Engenharia bovino e búfalos. Embrapa Pantanal. p.1-22. Boletim de Pesquisa Ambiental, vol. 6, no. 2, p. 620. e Desenvolvimento, no. 28. CORADIN, L., Org., 2006. Espécies exóticas invasoras: situação NASCIMENTO, FL., CATELLA, AC., MORAES, AE., 200l. brasileira. Brasília: Ministério do Meio Ambiente, Secretaria de Distribuição espacial do tucunaré, Cichla sp. (Pisces, Cichlidae), Biodiversidade e Florestas. 24 p. peixe amazônico introduzido no Pantanal, Brasil. Corumbá: Embrapa Pantanal, 17 p. Boletim de Pesquisa, no. 24. DARRIGAN, G. and PASTORINO, G., 1995. The recent introduction of Asiatic Bivalve, Limnoperna fortunei (Mytilidae) into South OLIVEIRA, MD., 2003. Ocorrência e impactos do Mexilhão America. The Veliger, vol. 38, no. 2, p. 183-187. dourado Limnoperna fortunei (Dunker, 1857) no Pantanal Mato-Grossense. Corumbá, MS: EMBRAPA. p. 6. Circular DARRIGAN, G. and PASTORINO, H., 2003. The golden mussel Técnica, no. 38. Limnoperna fortunei (Dunker, 1857) (Bivalvia: Mytilidae), in the Neotropical region: a 10-year story of invasion. Tentacle, -, 2004. Introdução de espécies: uma das maiores causas de perda no. 11, p. 8-9. de biodiversidade. Corumbá, MS: Embrapa Pantanal. p. 1-3. DESBIEZ, ALJ., SANTOS, SA., KEUROGHLIAN, A. and OLIVEIRA, MD., TAKEDA, AM., BARBOSA, DS. and BODMER, RE., 2009. Niche partitioning among white-lipped CALHEIROS, DF., 2000. Ocorrência da especie exótica peccaries (Tayassu pecari), Collared Peccaries (Pecari tajacu), Limnoperna fortunei (Bivalvia, Mytilidae) no Rio Paraguai, and Feral Pigs (Sus Scrofa). Journal of Mammalogy, vol. 90, Pantanal, Brasil. In: Resumos do III Simpósio Sobre Recursos no. 1, p. 119-128. Naturais e Socio‑Economicos do Pantanal. Os desafios do novo milênio. Corumba: Embrapa Pantanal. p. 264-265. FERRAZ DE LIMA, JA., 1993. Recursos Pesqueiros em ambientes inundáveis (rio Cuiabá: Pantanal de Mato Grosso). In: Anais do SANTOS, SA., CUNHA, CN., TOMÁS, W., ABREU, UGP. and ARIEIRA, J., 2006. Plantas invasoras no Pantanal: como Encontro Brasileiro de Ictiologia, 1993. Sociedade Brasileira de entender o problema e soluções de manejo por meio de diagnóstico Ictiologia, Universidade de São Paulo. participativo. EMBRAPA-Pantanal. 45 p. Boletim de Pesquisa e FINE, PVA., 2002. The invasibility of tropical forests by exotic Desenvolvimento, no. 66. plants. Journal of Tropical Ecology, vol. 18, no. 5, p. 687-705. SEGURA, MNO., MONTEIRO, HAO., LOPES, ES., SILVA, HARRIS, MB., TOMAS, W., MOURÃO, G., SILVA, CJ., OV., CASTRO, FC. and VASCONCELOS, PFC., 2003. Encontro GUIMARÂES, E., SONODA, F. and FACHIM, E., 2005. de Aedes albopictus no Estado do Pará, Brasil. Revista de Saúde Safeguarding the Pantanal Wetlands: threats and conservation Pública, vol. 37, no. 3, p. 388-389. iniciatives. Conservation Biology, vol. 19, no. 3, p. 714-720. SICURO, FL. and OLIVEIRA, LFB., 2002. Coexistence of peccaries Instituto Horus, 2009. Rota de dispersão do caramujo Achatina and feral hogs in Brazilian Pantanal wetland: an ecomorphological fulica introduzido no Brasil. Available from:

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A conservation agenda for the Pantanal’s biodiversity Alho, CJR.* and Sabino, J. Programa de Pós-graduação em Meio Ambiente e Desenvolvimento Regional, Universidade Anhanguera – Uniderp, CEP 79037-280, Campo Grande, MS, Brazil *e-mail: [email protected] Received October 14, 2010 – Accepted December 13, 2010 – Distributed April 30, 2011

Abstract The Pantanal’s biodiversity constitutes a valuable natural resource, in economic, cultural, recreational, aesthetic, scientific and educational terms. The vegetation plus the seasonal productivity support a diverse and abundant fauna. Many endangered species occur in the region, and waterfowl are exceptionally abundant during the dry season. Losses of biodiversity and its associated natural habitats within the Pantanal occur as a result of unsustainable land use. Implementation of protected areas is only a part of the conservation strategy needed. We analyse biodiversity threats to the biome under seven major categories: 1) conversion of natural vegetation into pasture and agricultural crops, 2) destruction or degradation of habitat mainly due to wild fire, 3) overexploitation of species mainly by unsustainable fishing, 4) water pollution, 5) river flow modification with implantation of small hydroelectric plants, 6) unsustainable tourism, and 7) introduction of invasive exotic species. Keywords: biodiversity, conservation, environmental threats, fauna, flora.

Uma agenda de conservação para a biodiversidade do Pantanal

Resumo A biodiversidade do Pantanal constitui recurso natural com reconhecido valor na economia, na cultura, na recreação, na estética, na ciência e na educação. A vegetação, mais a produtividade sazonal, suporta uma fauna abundante. Muitas espécies ameaçadas de extinção ocorrem na região e aves aquáticas são excepcionalmente abundantes durante a estação seca. Perdas da biodiversidade do Pantanal e de seus hábitats naturais associados ocorrem como resultado do uso não sustentável da terra. A implementação de áreas protegidas é somente uma parte da estratégia necessária. Analisamos as ameaças ambientais do bioma sob sete tópicos principais: 1) conversão da vegetação natural em pasto e campos agrícolas; 2) destruição e degradação de hábitats, principalmente pelo emprego de fogo; 3) sobre uso de espécies, principalmente pela pesca; 4) poluição de água; 5) modificação de fluxo de rios, principalmente pela implantação de pequenas usinas hidrelétricas; 6) turismo não sustentável; e 7) introdução de espécies invasoras exóticas. Palavras-chave: biodiversidade, conservação, ameaças ambientais, fauna, flora.

1. Introduction As a wetland, the Pantanal is a biome characterised by substrate and biota (Alho, 2005). Most of the Pantanal constant or recurrent shallow flooding near the surface of fauna is widely distributed and endemic species are rare the substrate, due to the low drainage capacity of its river in the biome (Brown-Junior, 1984; Junk et al., 2006, system. This is the most remarkable feature of the Pantanal, Lourival et al., 2000). with a dynamic that alternates annual cycles of droughts The Pantanal is also characterised by a high density and floods, and determines the ecological interactions and of various species of large vertebrates, with densities of patterns of biological diversity (Junk et al., 1989, 2006). populations that are not observed in any other biome in Brazil. The climatic and hydrological processes between plateau Inventories carried out by Conservation International‑Brazil and surrounding plains are essential to maintain this showed average densities of 4.3 for alligators, 1.8 for water system, a fact that qualifies the Pantanal biome as capybaras, and 0.3 for marsh deer per square kilometre, a complex and unique system. The flood plain comprises population concentrations that provide an enormous potential approximately 60% of the geographical extent of the Upper for ecotourism and wildlife management (Willink et al., Paraguay River Basin (Harris et al., 2005, 2006). Three 2000). Similarly as for birds and mammals, the region major factors characterise the Pantanal wetland: water, has many species of fish with high populations, especially

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 327-335 327 Alho, CJR. and Sabino, J. those whose food supply is based on organic material biome, including scientific research combined with (Britski et al., 2007; Fernandes et al., 2009). Additionally, labour‑management policies for scientific use and demographically healthy populations of many endangered conservation of biodiversity in NGOs and government species such as the Brazilian giant otter (Pteronura agencies, carried out in different regions within the brasiliensis), the jaguar (Panthera onca) and the greater considerable scale of time. hyacinth macaw (Anodorhynchus hyacinthinus) are still To list the endangered species in the Pantanal and viable in the Pantanal. These characteristics, combined surroundings, we consulted the IUCN Redlist (IUCN, with the high degree of conservation, are responsible for 2010, CR = Critical Endangered, EN = Endangered, the inclusion of the Pantanal in the National Heritage List VU = Vulnerable, NT = Near Threatened), and the official in the Brazilian Constitution of 1998 and the inclusion Brazilian List of Threatened Fauna (MMA, 2003) and of the biome in the Ramsar Convention on Wetlands of threatened fishes and invertebrates (MMA, 2004). International Importance (Willink et al., 2000; Alho, 2005); it is also considered one of the 37 major wilderness areas 3. Results and Discussion remaining on Earth (Mittermeier, 2002). The region is formed by a complex mosaic of different The major challenge for the Pantanal is to meet the kinds of habitats, strongly dependent on seasonal flooding. growing demand for social and economic development, The present landscape arrangement and natural ecosystems mainly cattle ranching, agriculture, urban growth and are the result of three factors: 1) evolutionary changes tourism, while conserving biodiversity and providing occurring since the Quaternary, which probably influenced essential ecosystem services for water quality, landscape the drainage patterns of the region; 2) the pronounced integrity and wildlife protection. differences in annual cycles of wet and dry seasons plus These challenges are aligned with the development exceptional periods of long flooding or droughts causing of new economic paradigms and environmental issues, retraction or expansion of the Pantanal, thus being a which require – in addition to scientific knowledge and new phenomenon related to greater or lesser primary productivity technologies – innovative business models that valorise and ecological succession and 3) areas involving human the natural capital and induce cultural changes. Natural intervention such as pastures, artificial ponds or introduced Capital – providing ecosystems and biodiversity benefits trees near the ranch houses (Alho, 2005). for humankind – clearly underlies everything. Yet the As seen throughout this volume on articles describing annual loss of land-based Natural Capital – in terms of the flora and fauna, the mixture of major vegetation lost human welfare benefits from forest loss alone – has formations that occur in the Pantanal has resulted in diverse reached US$ 2 trillion to US$ 4.5 trillion (TEEB, 2010). and abundant fauna. The species which are able to exploit Obviously, these innovative concepts are appropriate to a wide range of resources have become both widespread the Pantanal and models of environmental evaluation and locally abundant. should be customised for the region. The implementation of the Convention on Biological 3.1. Threats Diversity has continued since its conclusion in 1992 on The major conservation problems of the Pantanal the occasion of the UN Conference on Environment and floodplain originate on the plateaus. The surrounding Development in Rio de Janeiro. Although there are a number region has an important ecological role for the Pantanal, of conservation initiatives, including plans, programmes and as it serves as source areas for the animal species and is projects such as “Priority Areas and Actions for Biodiversity essential in the maintenance of hydrological processes and Conservation - Cerrado and Pantanal = Áreas e Ações the system of drought and floods (Brown-Junior, 1984; Prioritárias para Conservação da Biodiversidade - Cerrado Willink et al., 2000). Consequently, preservation of the e Pantanal” (MMA, 2007), a conservation synthesis on Pantanal is directly linked to preservation of the adjacent biodiversity status has been recently published worldwide Cerrado. New trends in economic development are shown (Millennium Ecosystem Assessment, 2005a-k). The third as the main threats to biodiversity in the Pantanal and its edition of Global Biodiversity Outlook (GBO‑3), produced surroundings (Alho, 2008a; Harris et al., 2005, 2006; Junk by the Convention on Biological Diversity (CBD) points and Cunha, 2005; Willink et al., 2000). Many farms have out that the world has failed to meet its target of achieving been established in the highlands surrounding the Pantanal a significant reduction in the rate of biodiversity loss and much of the natural vegetation (savanna) has been by 2010 (Secretariat of the Convention on Biological converted to soybean plantations or by other activities Diversity, 2010). (Alho, 2005; CI et al., 2009). Among these problems are The aim of this paper is to provide a concise review erosion, compacted soil, expansion of exotic pasture areas, of the Pantanal’s biodiversity conservation, discussing the silting rivers, pollution of water sources including by environmental threats and suggesting conservation needs. environmental contaminants (e.g. mercury), alterations in the water level, damming of rivers, and deposits of sewage 2. Methods and solid waste (Harris et al., 2005, 2006). This article is based on two approaches: 1) literature Deforestation, expanding agriculture, illegal fishing and review and 2) the experience of the authors with the hunting, unplanned tourism, and pollution by pesticides have

328 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 327-335 Conservation of the Pantanal’s biodiversity also caused a progressive deterioration of natural habitats. cattle ranching and agricultural activities, especially in Because of the huge demand for soybean plantations on the the highland region (CI et al., 2009). This study points upland plateaus surrounding the Pantanal, the application out that while the Pantanal maintains 86.6% of its natural of toxic agricultural chemicals is very common (Alho, vegetation, the surrounding upland plateaus (planaltos) 2005; Harris et al., 2005, 2006). have kept only 41.8% of their original vegetation cover. These environmental threats result in many endangered During the short period from 2002 to 2008, the Brazilian species, belonging to major taxa of Mammalia, Birds, side of the BAP lost 4% of its vegetation on the plateaus Reptilia, Actinopterygii, Bivalves and Lepidoptera (Table 1). and 2.4% in the floodplain (the Pantanal). Data for 2008 In the Pantanal, 20 species were from the official Brazilian show that cattle ranching is responsible for 11.1% of List of Threatened Fauna (MMA, 2004) and threatened vegetation conversion in the Pantanal and 43.5% in the fishes and invertebrates (MMA 2004), and the IUCN listed upland plateaus. four species in category “Endangered”, eight “Vulnerable” 3.1.2. Destruction or degradation of habitat mainly due and 17 “Near Threatened”, while in the surrounding to wild fire areas there were 22 species from the Brazilian List, and the IUCN showed one species “Critically Endangered”, Fire is a major threat. Ranchers in the Pantanal set fire two “Endangered”, seven “Vulnerable”, and 18 “Near to the vegetation during the dry season as a “management” Threatened” (Table 1). technique to “clear” the vegetation not used by cattle. The The environmental threats to the Pantanal’s biodiversity fire is initially started in the grassland but due to open can be grouped under seven interacting categories: areas, dry vegetation and wind, the fires often spread to 1) conversion of natural vegetation into pasture and savannas, woodland and forest (Alho, 2005). Removal of agricultural crops, 2) destruction or degradation of habitat natural vegetation eliminates food and shelter, especially for mainly due to wild fire, 3) overexploitation of species mainly forest-dwelling wildlife and epiphytic plants. Deforestation by unsustainable fishing, 4) water pollution, 5) river flow also increases erosion since most elevated areas have modification with implantation of small hydroelectric plants, sandy soil that is easily blown or washed away by rain. 6) unsustainable tourism, and 7) introduction of invasive 3.1.3. Overexploitation of species mainly by exotic species. More recently, two other factors have unsustainable fishing proven devastating to populations and ecosystems, adding to the list: pathogen pollution, and global environmental Deforestation also affects fish since migration may be change linked to climate (a direct effect on biodiversity influenced by terrestrial habitat disturbances, mainly gallery and human health related to climate change is the likely forests and seasonally flooded fields. In the “piracema” – a increase in infectious diseases transmitted by insects or kind of migration – the schools of fish move upstream at through contaminated water). the beginning of the rainy season. Other migratory fish species leave the riverbed and move into the adjacent 3.1.1. Conversion of natural vegetation into pasture and flooding areas searching for food. agricultural crops Species of large fish such as jaw characins (Salminus A study carried out to present the results of monitoring brasiliensis), spotted surubim (Pseudoplatystoma changes in vegetation and land use in the Brazilian part of corruscans), barred surubim (Pseudoplatystoma fasciatum), the Upper Paraguay River Basin (Bacia do Alto Paraguai) - streaked prochilod (Prochilodus lineatus), “piraputanga” BAP, (with a total area of 368,640 km²), considering the (Brycon hilarii) and threespot leporinus (Leporinus friderici) period from 2002 to 2008, showed that the region has are some of the most remarkable Pantanal ichthyofauna been suffering the consequences of the expansion in (Menezes, 1994). This is due, in part, to the size of these

Table 1. Number of threatened species for the Pantanal and surroundings, based on IUCN Redlist (CR – Critical Endangered, EN – Endangered , VU – Vulnerable, NT – Near Threatened), and official Brazilian List of Threatened Fauna and Threatened Fish and Invertebrates (MMA, 2003, 2004). Pantanal Surroundings Taxon CR EN VU NT MMA CR EN VU NT MMA Mammals 0 1 5 10 13 0 1 5 9 13 Birds 0 3 3 7 7 1 1 1 9 4 Reptiles 0 0 0 0 0 0 0 1 0 0 Fishes 0 0 0 0 0 0 0 0 0 2 Bivalves 0 0 0 0 0 0 0 0 0 2 Lepidoptera 0 0 0 0 0 0 0 0 0 1 Total 0 4 8 17 20 1 2 7 18 22

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 327-335 329 Alho, CJR. and Sabino, J. large fish species that are valuable for professional and 3.1.5. River flow modification with implantation of amateur fishing (Catella, 2004). Less evident and less known, small hydroelectric plants on the upland plateaus but no less important, are the small fish species, which are The floodplain is mainly formed by the tributaries from up to 15 cm in length. Without the small characins, small the left margin of the Paraguay River, in Brazil, with its catfish and small armored catfish, many large species could western border following that of Brazil itself, touching not exist: small species support aquatic food-chains, or are Bolivia to the north and Paraguay to the south. The streams food-chain links, and essentially are fish whose biological and rivers on these highlands are most prevalent where richness is yet to be adequately evaluated, especially in rainfall is ample, during the wet season. On the plateaus the headwaters of the Pantanal (Sabino and Prado, 2006). small brooks flow into small rivers, which flow into larger There is evidence of overfishing in some large fish ones. The large rivers are shaped mainly by terrain, velocity species (Garcia, 2006), a major threat hanging over the of the water, levels of dissolved oxygen, nutrient loads, water system of the Pantanal, which may adversely affect temperature and type of riverbed. The major rivers feeding the flood pulse of the plain. About 70% of the water of the Pantanal are (from north to south): Paraguay, Bento the Pantanal wetland originates in the northern part of the basin, and the Cuiaba River, forming the main tributary of Gomes, Cuiaba, São Lourenço-Itiquira, Taquari, Negro, the Pantanal, contributes 40% of the water system (Brasil, Aquidauana-Miranda, Nabileque and Apa. These rivers are 1997). Consequently, the information that 75% of all slow-moving when they meet the flatland and have coves 115 dam projects planned for the Upper Paraguay basin with adjacent flood-land. They periodically overflow their (BAP) are in the northern region, in Mato Grosso State banks. The maze of fluctuating water levels, nutrients, and (ANEEL, 2010), gives a glimpse of a disturbing scenario wildlife forms a dynamic ecosystem. Flood-lands cover since all these developments may change the hydrodynamics about 80% of the whole Pantanal. In contrast, during the and floods in the wetland plain (Girard, 2002). A simple dry season, most of the flooded areas stay dry, when the change in the regime of droughts and floods in this biome water returns to the river-beds (Alho, 2005, 2008a). has already produced worrying results, since the main In particular, these changes may threaten water trigger for the reproduction of fish is the rise in river level conservation in the main protected area and Ramsar with the first rains. Consequently, changes in this pattern Site, the Pantanal National Park. It is noteworthy that negatively affect the reproductive cycle. When the fish run three quarters of these enterprises involve small hydro into an insuperable obstacle and a lake, their reproductive power-plants (PCH, from Portuguese acronym), located cycle is not completed because spawning occurs in the or planned for the same river, together resulting in an upper river (Godinho et al., 2009). important impact. Even small power-plants, which may When dams are installed, conservation of the fish fauna, not form a reservoir, can change the discharge of nutrients particularly migratory species, requires that connectivity and suspended matter and hence the cycling of nutrients in is restored between the river channel and its flood areas affected water bodies (Calheiros et al., 2009; Fernandes, (wetlands). Additionally, they are eco-hydrological studies 2010). Furthermore, the presence of the physical barrier which would be required in each river to assess the flow in the form of a dam is known to prevent the movement rates, in the flood period, timing of the spawning migration of migratory fish species during the spawning season, period and to ensure the survival of juvenile forms of fish affecting fish production in the medium and long term (Calheiros et al., 2009). (Fernandes et al., 2009; Suzuki et al., 2009). All these 3.1.4. Water pollution changes and negative impacts on the water ecology of The introduction of toxins and other contaminants each sub-basin forming the Pantanal should be assessed to the Pantanal is an undesirable trend in habitat quality, simultaneously, in terms of the integrated area of the Upper since it affects valuable wildlife and fish resources as well Paraguay River Basin, prior to installing such projects as the quality of associated natural resources, including (Calheiros et al., 2009). surface and ground water. The introduction of pollutants 3.1.6. Unsustainable tourism to ecosystems results in changes in an interrelated series of variables or processes that can affect the structure and Tourism, if well planned and regulated, provides an function of the ecosystem in the short or long term. excellent alternative economy for the region. There is Alho and Vieira (1997) point out that unregulated gold a booming tourist trade in the Pantanal. Unfortunately, mining has contaminated Pantanal habitats with mercury. most of this tourism is predatory. Tour groups may invade Fish samples showed high percentages of contamination areas that should be preserved (e.g., waterfowl nesting (Cuiaba and Bento Gomes rivers) with mercury beyond the grounds or rookeries), sport fishing groups may over-fish, levels allowed by international standards for contamination. in general spreading litter, particularly in illegal camp Bird species, which feed on fish, like the olivaceous sites in gallery forest, where these fishermen leave signs cormorant Phalacrocorax olivaceu, the limpkin Aramus of their predatory presence. Numerous tourist hotel boats guarauna and the snail-kite Rosthramus sociabilis were throughout the Pantanal do not treat waste properly and also contaminated. spread solid waste on their way (Alho, 2005).

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3.1.7. Introduction of invasive exotic species is one of the most severe negative impacts on Exotic species introduction has been one of the most biodiversity. important factors of biodiversity loss in the region, as Traditionally, the conservation agenda employs the discussed in a specific chapter of this volume. implementation of conservation units in selected priority areas, with relevant biological attributes. This has been 3.2. Conservation agenda shown to be insufficient. The agenda needs to include Important comprehensive global analyses on biodiversity other approaches, such as economic incentives that would conservation and sustainable use have been produced induce stakeholders to adopt initiatives that balance and published: on the ecosystem and human well-being economic interest and nature protection. In the Pantanal (Millennium Ecosystem Assessment, 2005a-k); on the there is enormous potential for ecotourism or well-planned importance of biodiversity in human health (Chivian and tourism in the wild. Bernstein, 2008); on the implementation of the objectives Wildlife watching, particularly ecotourism, is a form of the Convention on Biological Diversity (Secretariat of of tourism based on the principles of making an active the Convention on Biological Diversity, 2010). contribution to the conservation of the natural and cultural Biodiversity plays a fundamental role as ecosystem legacy and interpreting the region’s natural and cultural services in the maintenance of natural ecological processes. heritage for visitors. Ecotourism­ is often based on relatively The economic or utilitar­ian values of biodiversity rely low levels of tourism in an area, and is therefore particularly upon the dependence of man on biodiversity, involving the suited to organised tours for small groups, and also for products that nature can provide: fishing resources, tourism independent travelers. In the Pantanal planning for this and extractive products. It also encompasses ecosystem kind of operation must increase to help local communities services, such as climate regulation, reproductive­ and generate sustainable income and employment. To be feeding habitats for commercial fish, some organisms sustainable, tourism needs to make a positive contribution that can create soil fertility through complex cycles and to the natural and cultural environment, generate benefits for interactions, such as earthworms, termites and bacteria, in the host communities, not put at risk the future livelihood of local people, and to make every effort to anticipate addition to the fungi responsible for cycling nutrients like and prevent economic, environmental, social and cultural nitrogen, phosphorus and sulfur and making them available degradation (Tapper, 2006). for plant absorption. These services are the benefits that Wildlife watching tourism in the Pantanal needs to people indirectly receive from natural ecosystem functions integrate considerations of sustainable development into (air quality maintenance, regional climate, water quality, the way in which it is operated and managed, and combine nutrient cycling, reproductive habitats of commercial fish, efforts for environmental education, including the construction etc.) with their related economic values (Alho, 2008b). of facilities for visitors, such as a public aquarium, thus The following conceptual levels of ecosystem are improving the structure of environmental interpretation. important in the Pantanal: Wildlife watching tourism also involves appropriately • Species diversity - the number of species found operated tourism activities that include local communi­ties, in a given study area or in a kind of habitat. wildlife managers in public and private sectors, national Although the species diversity of the Pantanal is and local government, conservation NGOs (particularly not high in comparison to other Brazilian biomes, wildlife societies which have a role in popularizing and the abundance of species, including endangered raising awareness­ about wildlife and conservation). The species, is high. tourism sector includ­es tour operators, local operators, • Functional diversity - the web of functions that are excursion providers, ac­commodation and, of course, the performed by species in a system, for example, tourists themselves (Cochrane, 2003; Tapper, 2006). the role of gallery forest for arboreal mammals, A wide range of recommendations should also be and the rhythms of seasonal production of food offered to managers of the environmental and water (shoots, flowers and fruits) for arboreal primates. resources of the two states in which the Pantanal is located Also includes feeding guilds of waterfowl (Mato Grosso and Mato Grosso do Sul), and managers observed in the Pantanal. of Brazilian electric sector. The decision makers need • Genetic diversity - genetic variability within a to be made aware of the fragility of the biome and the species, that is, variation among individuals or effect of changes in hydrological cycles arising from populations. construction of small dams for hydroelectricity. Among • Community and ecosystem diversity - assemblages the suggestions, particularly urgent is an Integrated of interacting different species also interacting Environmental Assessment on the impacts of the use of with abiotic components of the environment, such electric power from the Alto Paraguay (Calheiros et al., as the cordilheira habitat of the Pantanal. 2009). Reports focused on basins north of the BAP show • Habitat diversity - characteristics of a given area that the migration of fish was negatively affected at several where species, population and communities occur. points, compromising their reproduction and distribution The Pantanal has a great variety of different kinds in the Pantanal. When faced with unsatisfactory conditions of habitats. Alteration and loss of natural habitat for their survival, some fish species tend to decrease in

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 327-335 331 Alho, CJR. and Sabino, J. number or size and even disappear, especially migratory Water resources species (Calheiros et al., 2009). Based on the available 1) Develop mandatory requirements for integrated scientific information on the basin of the Upper Paraguay studies on environmental impact of large and Pantanal, specific guidelines for the sustainability of development projects, such as waterways. the region must be formulated (e.g., Conservation Plan 2) Secure the control of environmental contaminants, of the Upper Paraguay Basin - PCBAP, Fund for Global including pesticides, according to international Environment and Global Environment Facility - GEF Alto protocols. Paraguay, among others) for the conservation of ecological 3) Enforce the existing legislation on water resources, processes that govern the functioning of this biome. One including their springs. way to ensure the ecological processes of fish fauna is 4) Consider the hydrological basin and micro basin to keep some sub-basins of the BAP free from any dams as a conservation unit or ecosystem. (Calheiros et al., 2009). 5) Implement the effective participation of the Basin However, conservation involves combining both natural Committees in order to enforce legislation. ecosystems and human societies, and conservationists deal 6) Promote the conservation of wetlands that within with systems that are extremely complex and fragile, as is the framework of the Ramsar Convention. the case of the Pantanal. Sometimes, the urgent nature of Air pollution and climatic change the problem demands that the stakeholder take immediate 1) Establish shared management between action in their own interests, despite the risks inherent in Government agencies and civil society to control the lack of certainty about how best to proceed. wildfire. Protected areas are a basis of conservation policies and 2) Conduct technical training, environmental provide multiple benefits. There are over 120,000 designated education, and campaigns to prevent and combat protected areas covering around 13.9% of the Earth’s land wildfire. surface. Despite its importance, just 0.55% of an area of 3) Carry out environmental restoration in degraded 2 140,000 km - only in Brazil – of the Pantanal is protected areas for carbon absorption (carbon capture), by federal conservation units (Harris et al., 2006). among other benefits. On a global scale, there has been a positive assessment of the implementation of public policies on science and Biodiversity: conservation, research and technology for the use and conservation of biodiversity sustainable use (Millennium Ecosystem Assessment, 2003, 2005a-k). The 1) Promote the expansion of protected areas, ideally success of these actions was made possible by unprecedented to reach 10% of the region as intended by the international cooperation among taxonomists from a wide Government (40% of indirect use conservation range of research institutions and collections, including units and 60% of direct use). museums and herbaria, universities, botanical gardens 2) Secure land ownership in protected areas, the and collections of biological resources (Higushi, 2006). development of their management plan and its This is still a drop in the ocean, considering the challenges effective implementation, including the necessary facing the Pantanal and surroundings. Fortunately, recent staff. 3) Target priority incentives for the creation of investments, which include the creation of research private reserves (RPPN). programmes (e.g., Rede Centro-Oeste and SisBiota, from 4) Promote incentives for the implementation of the Ministry of Science and Technology, and Biota-MS ecological sales taxes (ICMS Ecológico). Programme, from Mato Grosso do Sul State) and institutions 5) Undertake the administration of bioregional areas (e.g., National Institute of Wetlands, the INAU) look set including the concept of ecoregions and biosphere to reverse this situation in Brazil. In the medium and long reserves. term, to expand and strengthen these coordinated scientific 6) Carry out experimental pilot projects for networks, it is necessary to build and maintain long-term sustainable use in protected areas of direct use. biodiversity research programmes in the Pantanal, based 7) Provide incentives for the creation of ex-situ on liaison between regional and national entities that work reserves. with biodiversity. 8) Provide incentives for sustainable use of biological Priority topics and guidelines for conservation: resources including wildlife. 9) Promote the certification of products from Environmental issues sustainable use programmes. Land use, soil conservation and management Scientific and technological issues 1) Promote agricultural practices for soil use that avoid loss of soil, including erosion. Research and technology 2) Promote economic activities related to the 1) Support shared participation between Government objectives of the protected areas’ buffer zones and and the private sector, aiming at the achievement experimental projects for extractive reserves. of innovative technologies.

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2) Promote basic and applied research for the 3) Create tourist facilities, such as public aquariums sustainable use of resources and technological and zoos, to disseminate biodiversity information practices for sustainable development. by means of environmental education programmes. Institutional issues Infrastructure 1) Harmonise planning and implementation of Institutional strength and shared management infrastructure, mainly for transport and energy, 1) Integrate information and actions of institutions with recommendations for ecological-economic engaged in conservation of the region. zoning, as well as undertaking reliable studies on 2) Promote government policies to implement environmental impact for each case. organisational strength including infrastructure, personnel, programmes and dissemination of References results. Legal and economic instruments Agência Nacional de Energia Elétrica - ANEEL, 2010. Quadro de acompanhamento de autorizações das PCH’s.I Ministério 1) Integrate sectoral policies in order to promote de Minas e Energia. Available from: http://www.aneel.gov.br/ regional conservation and development. aplicacoes/autorizacoes/default_aplicacao_acompanhamento. 2) Create incentives for shared environmental cfm?IDACOMPANHAMENTOTIPO=4. Access in: 25 jun. 2010. management at all levels. 3) Promote law enforcement. ALHO, CJR., 2005. The Pantanal. In: FRASER, LH. and KEDDY, PA., Org. The world’s largest wetlands - Ecology and conservation. 4) Implement ecological-economic zoning. New York, USA: Cambridge University Press. p. 203-271. Social-cultural issues -, 2008a. Biodiversity of the Pantanal: response to seasonal flooding regime and to environmental degradation. Brazilian Journal of Land use, territorial expansion with new agricul- Biology, vol. 68, no. 4, p. 957-966. Suppl. tural frontiers -, 2008b. The Value of Biodiversity. Brazilian Journal of Biology, Produce guidelines for implementing ecological- vol. 68, no. 4, p. 1115-1118. Suppl. economic zoning through shared participation and development indicators for sustainability. ALHO, CJR. and VIEIRA, LM., 1997. Fish and wildlife resources in the Pantanal wetlands of Brazil and potential disturbances Urban and metropolitan expansions from the release of environmental contaminants. Environmental Develop means to control urban migration. Toxicology and Chemistry, vol. 16, no. 1, p. 71-74. Poverty and life quality BRASIL, 1997. Ministério do Meio Ambiente, dos Recursos Hídricos e da Amazônia Legal. Secretaria de Coordenação Develop programmes to support health and dos Assuntos de Meio Ambiente. Programa Nacional do Meio education for better quality of life. Ambiente. Plano de conservação da Bacia do Alto Paraguai (Pantanal): PCBAP. Análise integrada e prognóstico da bacia Cultural diversity and traditions do Alto Paraguai. Brasília, DF: PNMA. 12 v. Recognise the value of ethno-cultural diversity BRITSKI, HA., SILIMON, KZS. and LOPES, BS., 2007. and traditional knowledge for conservation and Peixes do Pantanal – Manual de identificação. 2. ed. Corumbá: sustainable use of resources. EMBRAPA. p. 227. Communication and environmental education. BROWN-JUNIOR, K., 1984. Zoogeografia da região do Pantanal Plan, regulate and implement programmes on Mato-grossense. In: Anais do Simpósio sobre os Recursos Naturais environmental education to spread and consolidate e Sócio-Econômicos do Pantanal. Brasília, DF: EMBRAPA. the education process of local people and to p. 137-78. disseminate information through modern means CALHEIROS, D., ARNDT, E., RODRIGUEZ, EA. and of communication. SILVA, MCA., 2009. Influências de usinas hidrelétricas no funcionamento hidro-ecológico do Pantanal Mato-Grossense – Economic issues Recomendações. EMBRAPA. Documento, no. 102. Available from: http://www.cpap.embrapa.br/publicacoes/online/DOC102.pdf. Mineral exploitation Access in: 20 jun. 2010. 1) Conduct sustainable mining. CATELLA, AC., 2004. A pesca no Pantanal Sul: situação atual e 2) Create environmental certification for mining. perspectivas. Corumbá: EMBRAPA Pantanal. Documentos, no. 48. 3) Integrate the process of authorisation, law enforcement, and control of mining. CHIVIAN, E. and BERNSTEIN, A., Eds., 2008. How human health depends on biodiversity., New York: Oxford University Eco-business and sustainable tourism Press. 566 p. 1) Develop incentives for sustainable use of COCHRANE, J., 2003. Forging links between protected areas biodiversity. and the tourism sector: how tourism can benefit conservation. 2) Develop incentives for sustainable tourism. Paris: UNEP. p. 13-14. Available from: www.uneptie.org/tourism.

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 327-335 333 Alho, CJR. and Sabino, J.

Conservação Internacional - CI, Ecologia e Ação - ECOA, Biodiversity and its conservation in the Pantanal of Mato Grosso, Fundación AVINA, Instituto SOS Pantanal and WWF- Brasil, Brazil. Aqua Science, vol. 69, no. 3, p. 278-309. 2009. Monitoramento das alterações da cobertura vegetal e uso do solo na Bacia do Alto Paraguai Porção Brasileira. LOURIVAL, R., HARRIS, MB. and MONTAMBAULT, Available from: http://assets.wwfbr.panda.org/downloads/ JR., 2000. Introduction to the Pantanal, Mato Grosso do Sul, mapacoberturabaciaaltoparaguai_estudocompleto.pdf. Access Brasil. In WILLINK, PW., CHERNOFF. B., ALONSO. LE., in: 20 jul. 2010. MONTANBAULT, JR. and LOURIVAL EDS, R. A biological assessment of the aquatic eco-systems of the Pantanal, Mato Grosso FERNANDES, IM., MACHADO, FA. and PENHA, J., 2010. do Sul, Brazil. Washington, D.C.: Conservation International, Spatial pattern of a fish assemblage in a seasonal tropical wetland: p. 28-33p. effects of habitat, biomass, water depth, and distance from species sources. Neotropical Ichthyology, vol. 8, MENEZES, NA., 1994, Importância da ictiofauna dos ecossistemas no. 2, p. 289-298. aquáticos brasileiros. In: Cadernos dos Seminários Sobre Fauna Aquática e o Setor Elétrico Brasileiro: reuniões temáticas FERNANDES, R., AGOSTINHO, AA., FERREIRA, EA., preparatórias - COMASE. Rio de Janeiro: Eletrobrás. p. 7-13. PAVANELLI, CS., SUZUKI, HI., LIMA, DP. and GOMES, LC., 2009. Effects of the hydrological regime on the ichthyofauna of Millennium Ecosystem Assessment, 2003. Ecosystems and human riverine environments of the Upper Paraná River Floodplain. well-being: a framework for assessment. Washington, D.C.: Island Brazilian Journal of Biology, vol. 69, no. 2, p. 669-680. Suppl. Press. The millennium ecosystem assessment series. GARCIA, ICB., 2006, Influência da pesca seletiva sobre o -, 2005a. Ecosystems and human well-being: current state and comprimento médio de maturação em população de Dourado trends. vol. 1. Washington, D.C.: Island Press. The millennium (Salminus brasiliensis), Piraputanga (Brycon hilarii) e Curimbatá ecosystem assessment series. (Prohilodus lineatus) no Rio Miranda. Campo Grande: Universidade Federal de Mato Grosso do Sul – UFMS. 46 p. Dissertação de -, 2005b. Ecosystems and human well-being: scenarios. vol. 2. mestrado em ecologia e conservação. Washington, D.C.: Island Press. The millennium ecosystem assessment series. GIRARD, P., 2002. Efeito cumulativo das barragens no pantanal: mobilização para conservação das áreas úmidas do Pantanal e -, 2005c. Ecosystems and human well-being: policy responses. Bacia do Araguaia. Campo Grande, MS: Instituto Centro Vida. vol. 3. Washington, D.C.: Island Press. The millennium ecosystem 28 p. Relatório. Available from: http://www.riosvivos.org.br/ assessment series. dowloads/Efeito_cumulativo_barragens_Pantanal.pdf. Access -, 2005d. Ecosystems and human well-being: multiscale assessments. in: 22 jun. 2010. vol. 4. Washington, D.C.: Island Press. The millennium ecosystem GODINHO, AL., LAMAS, IR. and GODINHO, HP., 2009. assessment series. Reproductive ecology of Brazilian freshwater fishes. Environmental Biology of Fishes, vol. 87, p. 143-162. -, 2005e. Ecosystems and human well-being: our human planet: summary for decision-makers. vol. 5. Washington, D.C.: Island HARRIS, MB., TOMAS, WM., MOURÃO, GM., DA SILVA, Press. The millennium ecosystem assessment series. CJ., GUIMARÃES, E., SONODA, F. and FACHIM, E., 2005. Desafios para proteger o Pantanal brasileiro: ameaças e iniciativas -, 2005f. Ecosystems and human well-being: general synthesis. em conservação. Megadiversidade, vol. 1, no. 1, p. 156-164. Washington, D.C.: Island Press. The millennium ecosystem assessment series. HARRIS, MC., ARCÂNGELO, C., PINTO, ECT., CAMARGO, G., RAMOS-NETO, MB. and SILVA, SM., 2006. Estimativa da -, 2005g. Ecosystems and human well-being: biodiversity synthesis. perda de cobertura vegetal original na Bacia do Alto Paraguai e Washington, D.C.: Island Press. The millennium ecosystem Pantanal brasileiro: ameaças e perspectivas. Natureza e Conservação, assessment series. vol. 4, no. 2, p. 50-66. -, 2005h. Ecosystems and human well-being: disertification HIGUSHI, H., 2006. Biodiversidade: a megaciência em foco. synthesis. Washington, D.C.: Island Press. The millennium Academia Brasileira de Ciência and Sociedade Brasileira para ecosystem assessment series. o Progresso da Ciência. Curitiba, 2006. p. 15. Documento de -, 2005i. Ecosystems and human well-being: opportunities and reunião paralela à COP-08. IUBS - 29th General Assembly/Report of Activities/Annex 3. challenges for business and industry. Washington, D.C.: Island Press. The millennium ecosystem assessment series. IUCN, 2010. IUCN Red List of Threatened Species. Version 2009.1. Available from: www.iucnredlist.org. -, 2005j. Ecosystems and human well-being: wetland and water synthesis. Washington, D.C.: Island Press. The millennium JUNK, WJ.; BAYLEY, PB. and SPARKS, RS., 1989. The flood ecosystem assessment series. pulse concept in river – floodplain systems. In: DODGE, DP., Ed. Proceedings of the International Larger River Symposium -, 2005k. Ecosystems and human well-being: health synthesis. - LARS. Canadian Journal of Fisheries and Aquatic Sciences, Washington, D.C.: Island Press. The millennium ecosystem vol. 106, p. 110-127. assessment series. JUNK, WJ. and CUNHA, CN., 2005. Pantanal: a large South Ministério do Meio Ambiente – MMA, 2003. Lista das espécies da American wetland at a crossroads. Ecological Engineering, fauna brasileira ameaçadas de extinção. Instrução Normativa, no. 3. vol. 24, p. 391-401. -, 2004. Espécies ameaçadas de extinção e espécies sobreexplotadas JUNK, WJ., CUNHA, CN., WANTZEN, KM., PETERMANN, ou ameaçadas de sobreexplotação, os invertebrados aquáticos e P., STRÜSSMANN, C., MARQUES, MI. and ADIS, J., 2006. peixes. Instrução Normativa, no. 5.

334 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 327-335 Conservation of the Pantanal’s biodiversity

-, 2007. Biodiversidade do cerrado e pantanal: áreas e ações variations in the abundance of young-of-the year of migratory prioritárias para conservação da biodiversidade. Brasília: MMA/SBF. fishes in the Upper Paraná River floodplain: relations with 540 p. Série Biodiversidade, no. 17. hydrograpfic attributes. Brazilian Journal of Biology, vol. 69, no. 2, p. 649-660. Suppl. MITTERMEIER, RA., MITTERMEIER, CG., GIL, PA. and PILGRIM, J., 2002. Wilderness: Earth’s last wild places. : TAPPER, R., 2006. Wildlife watching and tourism: a study on CEMEX. 573 p. the benefits and risks of a fast growing tourism activity and its SABINO, J. and PRADO, PI., 2006. Vertebrados: síntese do impacts on species. Germany: UNEP/CMS Secretariat, Bonn. 68 p. conhecimento da diversidade biológica do Brasil. In: THOMAS, M. The Economics of Ecosystems and Biodiversity - TEEB, 2010. and LEWINSO, HN., Org. Avaliação do estado do conhecimento Report for business, executive summary 2010. United Nations da diversidade brasileira. Brasília: Ministério do Meio Ambiente. Environment Programme. p. 20. vol. 2, p. 55-143. WILLINK, PW., CHERNOFF, B., ALONSO, LE., Secretariat of the Convention on Biological Diversity, 2010. MONTANBAULT, JR. and LOURIVAL, R., 2000. A biological Global biodiversity outlook 3. Montreal. p. 94. assessment of the aquatic eco-systems of the Pantanal, Mato SUZUKI, HI., AGOSTINHO, AA., BAILLY, D., GIMENES, Grosso do Sul, Brazil, RAP. Bulletin of Biological Assessment, MF., JÚLIO-JUNIOR, HF. and GOMES, LC., 2009. Inter-annual vol. 18, p. 305.

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Concluding remarks: overall impacts on biodiversity and future perspectives for conservation in the Pantanal biome Alho, CJR.* Programa de Pós-graduação em Meio Ambiente e Desenvolvimento Regional, Universidade Anhanguera – Uniderp, CEP 79037-280, Campo Grande, MS, Brasil *e-mail: [email protected] Received October 14, 2010 – Accepted December 13, 2010 – Distributed April 30, 2011

Abstract The Pantanal biome is characterised by seasonal flooding which determines specific ecosystem processes, with the occurrence of adapted plants and animals to the annual shrinking and expansion of habitats due to the seasonal hydrological regime. Biodiversity abundance varies during the dry and wet seasons. The Pantanal’s biodiversity is a fundamental component of ecosystem services for human society, including nutrient cycling, fish production, ecotourism, carbon storage, flood control, among others, which are relevant to regional and global environmental consequences. The biome has been impacted by the conversion of natural vegetation into agricultural fields and pasture for cattle raising, with alteration and loss of natural habitats and biodiversity. Major negative impacts occur in uplands, with drastic deforestation of savanna vegetation, where main rivers feeding the Pantanal have their springs. This article discusses future needs and priorities for ecological research, in order to better understand the biome’s natural system, to achieve conservation and sustainable use. Keywords: biodiversity, conservation, environmental impacts, habitats, Pantanal.

Observações conclusivas: impactos ambientais sobre a biodiversidade e perspectivas futuras para conservação no bioma Pantanal

Resumo O bioma Pantanal é caracterizado pela inundação sazonal que determina processos ecossistêmicos específicos, com a ocorrência de plantas e animais adaptados à mudança anual de encolhimento e expansão de hábitats em virtude do regime hidrológico sazonal. A biodiversidade do Pantanal é um componente fundamental dos serviços ecossistêmicos prestados à sociedade humana, que inclui reciclagem de nutrientes, produção pesqueira, ecoturismo, resgate de carbono, controle de enchentes, entre outros, que são importantes consequências ambientais em nível regional e global. O bioma tem sido afetado pelo impacto da conversão de sua vegetação natural em campos agrícolas e pasto para a pecuária, com alteração e perda de hábitats e biodiversidade. O impacto maior tem ocorrido nas terras altas do planalto do entorno da planície, com desmatamento do Cerrado nas áreas onde nascem os rios que alimentam o Pantanal. Este artigo discute as necessidades e prioridades futuras de pesquisa ecológica para melhor entender o ecossistema e, assim, atingir sua conservação e uso sustentável. Palavras-chave: biodiversidade, conservação, impactos ambientais, hábitats, Pantanal.

1. Land Use The loss of natural habitats and their associated Pantanal still retains about 80% of its natural vegetation, biodiversity in the Pantanal have been drastic during the last but the upper reaches of the Paraguay River basin have lost decades, particularly in the upland region of the Cerrado about 60% of its natural vegetation cover, with a higher plateaus surrounding the flooding plain (Silva et al., 2010; rate of deforestation in the highland areas of the basin. Conservação Internacional, 2009). The study by Silva et al. Agriculture (mainly soybean) and cattle ranching is (2010) analysed the deforestation of the Pantanal and prevalent in highlands but in the northern region of the its surroundings over the past 30 years. Deforestation river basin, mining has been active since the beginning of in the Pantanal increased about 20 times in the period, the XVIII century (Casarin, 2007). Mining is responsible reaching near 15-20% of its area. Deforestation in the for environmental degradation in the region of the Upper Paraguay River Basin reached more than 40%. The Paraguay/Diamantino watershed, resulting in erosion

Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 337-341 337 Alho, CJR. with revolved soil due to mining processing. In addition, 2. Research Priorities deforestation for agriculture and cattle pasture cause It has become evident, because of the importance of erosion mainly in slope terrains and mountain hillsides of the highlands. the Pantanal biome, that scientific research is needed to While at the international level, the Ramsar Convention improve conservation on the basis of scientific methods, on Wetlands was established to protect wetlands, on in order to discuss the progress, problems and priorities to the national level, Brazil has signed the Convention achieve sustainable use in the region. Scientific research and designated the Pantanal as a Ramsar site. On the improves our understanding of the magnitude of biodiversity, other hand, Brazilian environmental legislation has been land use, and contributes to mitigating land use impacts. recognised as updated, but difficult to enforce due to a Incorporating research results into an action plan for weak environmental institutional structure, mainly in the biodiversity conservation of the Pantanal is an important two states (Mato Grosso and Mato Grosso do Sul) which part of the adaptive management process. The following comprises the Pantanal. are identified research priority topics for science-based conservation, protection and management: 1.1. Environmental impacts affecting biodiversity • Studies on ecological processes to better The Pantanal has been negatively impacted by understand the function of natural ecosystems; unsustainable socio-economic development through • Hydrology studies to establish the relationship predatory land use (Alho, 2005). Major economic activities and dependence of river flow from highlands to are cattle ranching, fishing, agriculture, mining and tourism. floodplain in connection to the kinds of habitats Deforestation to convert natural habitats with pastures for and their associated biodiversity; cattle is increasing. The consequence is loss of biodiversity, • Studies on fish movement, dispersal of for example, removal of forest that eliminates food and semi‑aquatic and aquatic mammals and other shelter, for forest-dwelling wildlife. Environmental pollutants organisms, in relation to flooding regime to are introduced from uncontrolled use of pesticides and determine their significance and sensitivity herbicides, contamination with mercury from unregulated to hydrological seasonal events and offer of gold mining, urban liquid and solid waste, including ecological resources; untreated sewage, introduction of invasive exotic species, • Emphasis on the magnitude of the biodiversity, unsustainable tourism, illegal hunting, traffic of wildlife, including ecological parameters such as species soil degradation, lack of education and environmental richness and species diversity of all types of wild consciousness, and fragility of environmental organizations plants and animals; to enhance legislation. • Studies on habitats and microhabitats requirements 1.2. Needs to identify, evaluate and mitigate and selection for wildlife in relation to seasonal environmental impacts offer of resources; Future development projects that affect the biome’s • Conservation action including protected areas, biodiversity should only be undertaken after proper and ecological corridors; feeding and reproductive thorough environment assessment procedures, based niches of wildlife; on specific terms of reference and public participation. • Effects of habitat heterogeneity and other Establishment of scoping to identify which potential impacts landscape factors on demography and recruitment are relevant to assess, based on legislation, international of indicator species of insects, herpetofauna, fish, conventions, technical and scientific knowledge and public birds and mammals; involvement, to correct analysis to license projects or to • Need to understand the effect of ecological reject them. processes on biodiversity responses (ecological Brazilian public attitudes toward nature in general, parameters and behavioural patterns) to factors and biodiversity in particular, have improved, and there measured in different kinds of habitats and at has been more drive to protect the Pantanal. It would landscape scales; constitute progress to protect the ecological relationship • Dispersal movements of wildlife, including fish, between the floodplain, which is the Pantanal, and its amphibians, reptiles, birds and mammals between surrounding upland plateaus, to apply environmental feeding niches and reproductive niches as a flow assessment (EFA) in any development project that function of seasonal annual variation; affects river flow. This should apply for the hydroelectric • Migration routes especially of bird species; plants being established in rivers that feed the Pantanal. • Studies on feeding and reproductive guilds of This procedure should determine how much of the natural birds and bats; flow regime of a given river should continue to flow down • Habitat selection and microhabitats of small to the Pantanal floodplain in order to maintain ecosystem mammals (rodents and marsupials); processes. If on the one hand, development projects are • Studies on environmental components selected by good for the region, on the other, conservation priorities small mammals in relation to habitat selection and have to be carried out in order to fulfill ecological needs. microhabitat types;

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• Identification and analyses of bioindicators for of natural habitats, the Pantanal is also facing other threats habitat quality and for degrees of disturbances; including the consequences of climate change. • Studies on ecological communities structure and Independent of human benefit or intervention, an function in relation to ecological processes of the ecosystem works as an interdependent system in nature Pantanal; and biodiversity is an important component of this holistic • Considerations on consumptive and non- system. However, during recent years, several published consumptive activities in the Pantanal as a means reports emphasise the role of ecosystem services for of improving ecotourism to achieve sustainable human being as a tool to apply conservation and protection use of the biodiversity. (Costanza et al., 1997; Daily, 1997; Daily et al., 1997; • Identification and evaluation of impacts and Balmford et al., 2002; De Groot et al., 2002; Millenium development of alternatives, to predict and identify Ecosystem Assessment, 2005a-k; Alho, 2008; Chivian environmental impacts of proposed projects; and Bernstein, 2008; Mindell, 2009; Keddy et al., 2009; • Monitoring, enforcement and environmental Cardinale et al., 2009). The concept of ecosystem services auditing mitigation projects to verify the implies function and ecosystem processes, meaning the compliance of proponents to ensure mitigation conditions through which natural ecosystems and biodiversity, and compensation impacts according to Federal that integrates the system, sustain and fulfill human life. and State legislation; Ecosystem services are the benefits provided to humans • Impact of invasive exotic species on population, as a function of ecosystem processes, like water quality, community and ecosystem structure and function; pure air, geobiochemical cycling of nutrients for plants • Identification and analysis of categories of and animals including importance for agriculture, wood, activities known to cause biodiversity impacts food, medicine and so on. It is the capacity of ecosystem including ecotourism; processes to provide services and goods that satisfy human • Studies on priority areas for conservation, needs. These ecosystem processes are interactions among including production of maps indicating elements of the ecosystem or ecological attributes (physical, conservation categories according to Brazilian like solar energy and soil; chemical, like photosynthesis legislation; areas where impact assessment at an and cycling of nutrients; biotic, like primary production appropriate level is required; areas containing and secondary production, food chain and behavioral threatened ecosystems outside of formally interactions) that are valued by humans. protected areas; areas identified as being important The following ecosystem services of the Pantanal for the maintenance of key ecological processes; illustrate the importance of protected nature and show areas known to be habitat for threatened species; the relevance for scientific research: areas identified as important cultural and spiritual • River flow. Natural river flows of hydrological components. cycles are fundamental for drainage, river • Establishment of the cause and effect relationship discharge and seasonal inundation that influence between land use activities and biodiversity, habitats and biodiversity. They provide water with focus on: indicator species, human-caused quality for human consumption and nutrients for impacts and aquatic integrity (macro-invertebrates fishery. as indicators); fish habitats and fishery; aquatic • Nutrient cycling. Carbon, oxygen, hydrogen, and semi-aquatic mammal species and dispersal nitrogen, phosphorus are cycled in ecosystems. in function of flooding regime; water quality Decomposition by soil organisms releases these indicators, and other contaminant indicators in and other elements into the soil and atmosphere so relation to aquatic health; they can be used again. Nutrient cycling provides • Establishment of benchmark conditions for productive soil. Ecological processes play a role in regional sustainable development indicators for storing and recycling organic matter, nutrients and ecotourism and recreational areas; human waste. • Research on climate change related risks in relationship to biodiversity and ecosystem • Fishery. Fish is an important economic element of integrity. the Pantanal. Feeding and reproductive habitats of commercial fish depend on natural ecosystems. 2.1. Ecosystem services in connection with human • Aesthetic, recreation and cultural attributes. well‑being and research opportunities There is an increasing touristic industry in the Ecosystem processes of the Pantanal maintain Pantanal. People are attracted to the region by biodiversity by providing habitats for many plant and its natural scenery and beautiful landscapes. Bird animal species. These processes produce products such as watching has become internationally popular in fish and other extractive resources. As a wetland, the biome the region and natural ecosystems are often used is a productive ecosystem, providing seasonal nutrients as places for recreation, including sport fishing. for biodiversity. In addition to unsustainable land use and The biome also offers cultural traditions and increasing economic development resulting in degradation folklore.

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• Medicinal and genetic attributes. The biome’s to human quality of life. This important Brazilian biome biodiversity offers a diversity of life forms to be requires sustainable management for its use and economic cultivated as crops and domesticated animals and development, built on a new approach for the future, also material for biotechnological experiments. considering the inseparable relationship between economic It provides material for synthetic drugs used as development and human well-being to achieve sustainability. medicines. Scientific research can pave the way to reach this objective. • Natural habitats and biodiversity. The Due to the rapid rate of environmental degradation, Pantanal’s natural systems provide living space including altered hydrology, with loss of natural habitats for plants and animals which characterise and biodiversity, management strategies are imperative its exuberant biodiversity, including genetic and urgent. diversity. The different kinds of vegetation cover provide suitable shelters and other ecological References resources to support a diversity of animal life. The heterogeneity of life forms is essential ALHO, CJR., 2005. The Pantanal. In LAUCHLAN, HF. and for maintaining all other ecosystem functions PAUL, AK., Org. The world’s largest wetlands – Ecology and and services, as a result of millions of years of conservation. New York, USA: Cambridge University Press. biological evolution. Maintenance of biodiversity p. 203-271. is supported by natural ecosystems within such -, 2008. The value of biodiversity. Brazilian Journal of Biology, a large biome as is the case of the Pantanal. The vol. 68, no. 4, (Suppl.), p. 1115-1118. biome’s current order of its biodiversity magnitude BALMFORD, A., BRUNER, A., COOPER, P., COSTANZA, depends upon its size (near 140,000 km²) and the R., FARBER, S., GREEN, RE., JENKINS, M., JEFFERISS, heterogeneity of its different kinds of natural P., JESSAMY, V., MADDEN, J., MUNRO, K., MYERS, N., habitats. Vegetation cover prevents soil erosion NAEEM, S., PAAVOLA, J., RAYMENT, M., ROSENDO, and sediment control. It also works on fixation of S., ROUGHGARDEN, J., TRUMPER, K. and TURNER, RK., solar energy and biomass production. 2002. Economic reasons for conserving wild nature. Science, • Scientific attributes. The Pantanal offers vol. 297, p. 950-953. numerous opportunities for scientific research, CARDINALE, BJ., SRIVASTAVA, DS., DUFFY, JE., WRIGHT, environmental education and monitoring JP., DOWNING, AL., SANKARAN, M., JOUSEAU, C., CADOTTE, environmental changes due to human occupation MW., CARROLL, IT., WEIS, JJ., HECTOR, A. and LOREAU, and impacts of development projects. M., 2009. Effects of biodiversity on the functioning of ecosystems: • Climate change. Vegetation cover, evaporation, summary of 164 experimental manipulations of species richness. regional and continental circulation patterns, like Ecology, vol. 90, no. 3, p. 854. Ecological Archives E090-060. El Niño and La Niña, and water bodies, all interact CASARIN, R., 2007. Caracterização dos principais vetores to determine weather and climate. Seasonally de degradação ambiental da bacia hidrográfica Paraguai/ flooded areas can be carbon sinks, which Diamantino. Rio de Janeiro: Instituto de Geociências, Programa influence global climate change. The regional soil de Pós-Graduação em Geografia, Universidade Federal do Rio is composed of partially decayed accumulations de Janeiro. 169 p. Tese de doutotado em geografia. of plants, and other organisms, resulting in CHIVIAN, E. and BERNSTEIN, A., Ed., 2008. How human stored carbon. The removal of carbon from the health depends on biodiversity. New York: Oxford University atmosphere depends on that carbon storage and Press. 566 p. vegetation cover. Estimates for the annual carbon Conservação Internacional – CI, Ecologia e Ação – ECOA, accumulation in the Pantanal are not known, Fundacíon AVINA, Instituto SOS Pantanal and WWF-Brasil. but the biome may play a significant role in the 2009. Monitoramento das alterações da cobertura vegetal e uso sequestration of carbon. There is a concerning do solo na bacia do alto Paraguai – Porção brasileira – Período de trend about the future of Brazilian biomes análise: 2002 a 2008. Brasília. 58 p. Relatório técnico metodológico. regarding climate changing and the ecosystem COSTANZA, R., D’ARGE, R., DE GROOT, R., FARBER, processes. According to the United Nations S., GRASSO, M., HANNON, B., LIMBURG, K., NAEEM, S., Climate Change Conference held in Cancún, O’NEILL, RV., PARUELO, J., RASKIN, RG., SUTTON, P. and Mexico, in November-December 2010, studies VAN DEN BELT, M., 1997. The value of the world’s ecosystem on climate and hydrologic models in the Cerrado services and natural capital. Nature, vol. 387, p. 253-260. river basins pointed out toward a reduction of DAILY, GC., ALEXANDER, S., EHRLICH, PC., GOULDER, L., 20‑25% of annual precipitation in 2100, leading to LUBCHENCO, J., MATSON, PA., MOONEY, HA., POSTEL, a decrease of 7-10% in the volume of recharge of S., SCHNEIDER, SH., TILMAN, D. and WOODWELL, GM., aquifers and in the river discharges, depending on 1997. Ecosystem services: benefits supplied to human societies the analysed scenario. by natural ecosystems. Washington, D.C.: Ecological Society Ecosystem services provided by the Pantanal include of America. maintenance of biodiversity, landscape, freshwater supply, DAILY, GC., Ed, 1997. Nature’s services: societal dependence fishery, nutrient cycling. These ecosystem services contribute on natural ecosystems. Washington, D.C.: Island Press.

340 Braz. J. Biol., 2011, vol. 71, no. 1 (suppl.), p. 337-341 Overall impacts on biodiversity of the Pantanal

DE GROOT, RS., WILSON, MA. and BOUMANS, RMJ., 2002. -, 2005f. Ecosystems and human well-being: general synthesis. A typology for the classification, description, and valuation of Washington, D.C.: Island Press. The millennium ecosystem ecosystem functions, goods, and services. Ecological Economics, assessment series. vol. 41, p. 393-408. -, 2005g. Ecosystems and human well-being: biodiversity synthesis. KEDDY, PA., FRASER, LH., SOLOMESHCH, AI., JUNK, WJ., Washington, D.C.: Island Press. The millennium ecosystem CAMPBELL, D., ARROYO, TK., ALHO, CJR., 2009. Wet and assessment series. wonderful: the world’s largest wetlands are conservation priorities. BioScience, vol. 59, no. 1, p. 39-51. -, 2005h. Ecosystems and human well-being: disertification Millennium Ecosystem Assessment, 2003. Ecosystems and human synthesis. Washington, D.C.: Island Press. The millennium well-being: a framework for assessment. Washington, D.C.: Island ecosystem assessment series. Press. The millennium ecosystem assessment series. -, 2005i. Ecosystems and human well-being: opportunities and -, 2005a. Ecosystems and human well-being: current state and challenges for business and industry. Washington, D.C.: Island trends. vol. 1. Washington, D.C.: Island Press. The millennium Press. The millennium ecosystem assessment series. ecosystem assessment series. -, 2005j. Ecosystems and human well-being: wetland and water -, 2005b. Ecosystems and human well-being: scenarios. vol. 2. synthesis. Washington, D.C.: Island Press. The millennium Washington, D.C.: Island Press. The millennium ecosystem ecosystem assessment series. assessment series. -, 2005k. Ecosystems and human well-being: health synthesis. -, 2005c. Ecosystems and human well-being: policy responses. Washington, D.C.: Island Press. The millennium ecosystem vol. 3. Washington, D.C.: Island Press. The millennium ecosystem assessment series. assessment series. MINDELL, DP., 2009. Environment and health: humans need -, 2005d. Ecosystems and human well-being: multiscale assessments. vol. 4. Washington, D.C.: Island Press. The millennium ecosystem biodiversity. Science, vol. 323, no. 5921, p. 1562-1563. assessment series. SILVA, JSV., ABDON, MM. and MORAES, JA. 2010. -, 2005e. Ecosystems and human well-being: our human planet: Desmatamento na bacia do Alto Paraguai no Brasil. In Anais do summary for decision-makers. vol. 5. Washington, D.C.: Island III Simpósio de Geotecnologias no Pantanal. 16-20 out. 2010, Press. The millennium ecosystem assessment series. Cáceres, MT. Embrapa Informática Agropecuária/INPE. p. 458-467.

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